Soil Collembolan Folsomia Candida Research Articles

A new insight into the potential drivers of antibiotic resistance gene enrichment in the collembolan gut association with antibiotic and non-antibiotic agents

Effects of non-antibiotic pharmaceuticals on antibiotic resistance genes (ARGs) in soil ecosystem are still unclear. In this study, we explored the microbial community and ARGs variations in the gut of the model soil collembolan Folsomia candida following soil antiepileptic drug carbamazepine (CBZ) contamination, while comparing with antibiotic erythromycin (ETM) exposure. Results showed that, CBZ and ETM all significantly influenced ARGs diversity and composition in the soil and collembolan gut, increasing the relative abundance of ARGs. However, unlike ETM, which influences ARGs via bacterial communities, exposure to CBZ may have primarily facilitated enrichment of ARGs in gut through mobile genetic elements (MGEs). Although soil CBZ contamination did not pose an effect on the gut fungal community of collembolans, it increased the relative abundance of animal fungal pathogens contained therein. Soil ETM and CBZ exposure both significantly increased the relative abundance of Gammaproteobacteria in the collembolan gut, which may be used to indicate soil contamination. Together, our results provide a fresh perspective for the potential drivers of non-antibiotic drugs on ARG changes based on the actual soil environment, revealing the potential ecological risk of CBZ on soil ecosystems involving ARGs dissemination and pathogens enrichment.

Toxic effects of norfloxacin in soil on fed and unfed Folsomia candida (Isotomidae: Collembola) and on gut and soil microbiota

Soils contaminated with antibiotics may exert effects on soil-dwelling animals. A systematic ecological toxicity assessment of norfloxacin on the soil collembolan Folsomia candida (F. candida) was therefore conducted in soil and Petri dish systems with and without feeding at the population, individual and cellular levels. The indicators survival, reproduction, antioxidant enzyme activities peroxidase (POD), catalase (CAT), and superoxide dismutase (SOD), malondialdehyde (MDA) contents and gut microbiota were studied. The surrounding soil microbiota were also investigated because F. candida can ingest soil microbiota that may have effects on the gut microbiota. In general, the toxicity of norfloxacin to F. candida in contaminated soil without food addition was higher than in contaminated soil with food addition. Norfloxacin had little effect at population and individual levels but antioxidant enzyme activities changed significantly in treatments with longer exposure times or higher norfloxacin concentrations. CAT was more sensitive than SOD or POD. The diversity indices and composition at phylum level of the gut microbiota showed little change. However, the operational taxonomic units in the gut decreased in the presence of norfloxacin. The relative abundance of Wolbachia, the predominant bacterial genus in the gut, decreased significantly with increasing soil norfloxacin concentration. Wolbachia may therefore be a promising bioindicator in the assessment of norfloxacin pollution of soils at environmental concentrations.

Exposure of a Soil Collembolan to Ag Nanoparticles and AgNO3 Disturbs Its Associated Microbiota and Lowers the Incidence of Antibiotic Resistance Genes in the Gut.

Gut microbiota contribute to host health. Numerous recent studies have focused on the survival and reproduction of nontarget soil animals exposed to the toxicity of silver nanoparticles (AgNPs) but changes in the gut microbiota due to nanoparticle toxicity are largely unknown. Here, we examine some effects of AgNPs and silver nitrate (ionic Ag) on the gut microbiota of the common soil collembolan Folsomia candida using Illumina sequencing and concomitant changes in antibiotic resistance genes (ARGs) of the gut microbiota using high-throughput quantitative PCR. A large number of Ag accumulated in Ag-exposed individuals after 28 days and ionic Ag significantly inhibited the reproduction of the collembolan (by 19.3%). Exposure to AgNPs disturbed the composition of the collembolan gut bacterial community, resulting in dysbiosis of the gut microbiota. However, the dominant microbiota was shared among different treatments. In addition, AgNPs exposure did indeed reduce the incidence of ARGs in the collembolan gut microbiota. A weak relationship was identified between gut bacterial communities and ARG profiles. These results extend our knowledge regarding the role of the gut microbiota in assessing the soil ecotoxicology of AgNPs.

Antibiotics Disturb the Microbiome and Increase the Incidence of Resistance Genes in the Gut of a Common Soil Collembolan.

Gut microbiota make an important contribution to host health but the effects of environmental pressures on the gut microbiota of soil fauna are largely uncharacterized. Here, we examine the effects of norfloxacin and oxytetracycline on the gut microbiome of the common soil collembolan Folsomia candida and concomitant changes in the incidence of antibiotic resistance genes (ARGs) in the gut and in growth of the collembolan. Exposure to 10 mg antibiotics kg-1 for 2 weeks significantly inhibited the growth of the collembolan with roughly a 10-fold decrease in 16S rRNA gene abundance. Antibiotics did alter the composition and structure of the collembolan gut microbiome and decreased the diversity of the gut bacteria. A decline in the firmicutes/bacteroidetes ratio in the antibiotic-treated collembolans may be responsible for the decrease in body weight. Exposure to antibiotics significantly increased the diversity and abundance of ARGs in the collembolan gut. The Mantel test and Procrustes analysis both reveal that ARGs and gut microbiota were significantly correlated with one another ( P < 0.05). These results indicate that antibiotics may induce a shift in the gut microbiota of nontarget organisms such as soil collembolans and thereby affect their growth and enrichment of ARGs.

Exposure of soil collembolans to microplastics perturbs their gut microbiota and alters their isotopic composition

Effects of microplastics on aquatic organisms have been widely studied in recent years but effects on soil biota, and especially on the gut microbiota of soil animals, remain poorly understood. An experiment was therefore conducted using the common soil collembolan Folsomia candida exposed to microplastics for 56 days to investigate the effects of plastics on gut microbiota, growth, reproduction and isotopic turnover of collembolans in the soil ecosystem. A diverse microbial community was observed in the collembolan gut, consisting of (at phylum level) Actinobacteria (∼44%), Bacteroidetes (∼30%), Proteobacteria (∼12%) and Firmicutes (∼11%). Distinctly different bacterial communities and lower microbial diversity were found in the collembolan gut compared with the surrounding soil. We also found that exposure to microplastics significantly enhanced bacterial diversity and altered the microbiota in the collembolan gut. Moreover, collembolan growth and reproduction were significantly inhibited (by 16.8 and 28.8%, respectively) and higher δ15N and δ13C values were observed in the tissues after exposure to microplastics. These results indicate that exposure to microplastics may impact non-target species via changes in their microbiota leading to alteration of isotopic and elemental incorporation, growth and reproduction. The collembolan gut microbial data acquired fill a gap in our knowledge of the ecotoxicity of microplastics.

Biomarker responses reveal that food quality affects cadmium exposure in the soil collembolan Folsomia candida

Food quality affects the food consumption rate, flux through the gut, and exposure to contaminants in animals. This study evaluated the effects of food quality on cadmium exposure in the soil collembolan Folsomia candida. Animals were exposed to constant concentrations of cadmium for 38 h via artificial food consisting of an agar medium with various concentrations of sugar (glucose), total nutrients (baker's yeast), or fungal odour (1-octen-3-ol). The expression of the gene encoding a deduced metallothionein-like motif containing protein was used as a biomarker of cadmium exposure. Glucose concentrations of 2% or higher reduced the expression levels of the biomarker. Within the range of 0.1–8% yeast, medium concentrations led to higher biomarker levels. At high concentrations of 1-octen-3-ol (2000 mg/l), feeding and the biomarker response were reduced. These results suggest that even at equivalent cadmium concentrations, food quality affects cadmium exposure by altering food consumption rates.

Laboratory assessment of the impacts of transgenic Bt rice on the ecological fitness of the soil non-target arthropod, Folsomia candida (Collembola: Isotomidae)

Transgenic rice expressing Bacillus thuringiensis (Bt) endotoxins (Bt rice) for pest control is considered an important solution to food security in China. However, tests for potential effects on non-target soil organisms are required for environmental risk assessment. The soil collembolan Folsomia candida L. (Collembola: Isotomidae) is a potential non-target arthropod that is often used as a biological indicator in bio-safety assessments of transgenic crops. In the present study, the roots, stems, and leaves of Bt rice were exposed to F. candida under laboratory conditions, with survival, reproduction and growth of the collembolan as ecological fitness parameters. Significant differences in ecological fitness were found among the different treatments, including differences in the plant parts and varieties of non-Bt rice, presumably as the result of three factors: gene modification, plant parts and rice varieties. The fitness of F. candida was less affected by the different diets than by the exposure to the same materials mixed with soil. Our results clearly showed that there was no negative effect of different Bt rice varieties on the fitness of F. candida through either diet or soil exposure.

Role of soil properties in sewage sludge toxicity to soil collembolans

Abstract Soil properties are one of the most important factors explaining the different toxicity results found in different soils. Although there is knowledge about the role of soil properties on the toxicity of individual chemicals, not much is known about its relevance for sewage sludge amendments. In particular little is known about the effect of soil properties on the toxicity modulation of these complex wastes. In addition, in most studies on sewage sludges the identity of the main substances linked to the toxicity and the influence of soil properties on their bioavailability remains unknown. In this study, the toxicity of a sewage sludge to the soil collembolan Folsomia candida was assessed in nine natural soils from agricultural, grassland and woodland sites, together with the OECD soil. Correlations between the relative toxicity of sludge for collembolans in the different soils and their physical and chemical soil properties were assessed in order to identify the main compounds responsible for the effects observed. Furthermore, the relationships between the toxic effects to collembolans and water-soluble ions released by sludge, pH and electric conductivity were also assessed, together with the modulating effects of soil properties. Sludge toxicity was directly linked to the water extractable ammonium, which explained most of the mortality of the collembolans, and part of the inhibition of reproduction. For the last endpoint, nitrite also contributed significantly to the inhibition observed. The varied levels in water extractable ammonium in the different soils at equal dosages seem to be, in turn, modulated by some soil properties. Higher organic carbon contents were associated with lower toxicity of sludge, both for survival and reproduction, probably related to its higher ammonium sorption capacity. In addition, for reproduction, increasing the C/N ratio and pH appeared to increase the toxicity, probably due to both the greater difficultly in nitrification and the known unsuitability of alkaline soils for this species.

MRNA expression of a cadmium-responsive gene is a sensitive biomarker of cadmium exposure in the soil collembolan Folsomia candida

The gene expression of environmental organisms is useful as a biomarker of environmental pollution. One of its advantages is high sensitivity. We identified the cDNA of a novel cadmium-responsive gene in the soil collembolan Folsomia candida. The deduced protein, designated “metallothionein-like motif containing protein” (MTC), was cysteine-rich and contained a metallothionein-like motif with similarity to metallothionein, but had a much longer sequence than metallothionein and contained repeated sequences of amino acids. Expression of MTC mRNA was sensitively induced by cadmium exposure at 0.3 mg/kg of dry food, a concentration at which toxic effects are not observed, but expression was not affected by γ-ray exposure (an inducer of oxidative stress). These findings suggest that MTC is involved in cadmium-binding processes rather than in oxidative-stress responses. In conclusion, we suggest that gene expression of MTC may be a candidate biomarker for detecting low levels of cadmium contamination in soil.

Feeding inhibition in the soil collembolanFolsomia candidaas an endpoint for the estimation of organic waste ecotoxicity

Despite the increasing quantities of organic wastes that are being reused in soils, there are few studies that focus on the selection of bioassays for the ecotoxicological risk assessment of organic wastes to soils. In the present study, differences in feeding inhibition in the soil collembolan Folsomia candida were evaluated as an ecotoxicological endpoint for the assessment of risk to soils amended with polluted organic wastes. Seven organic wastes (dewatered sewage sludges, thermally dried sewage sludges, composted sewage sludges, and a thermally dried pig slurry) were tested. These wastes had different origins, treatments, and pollutant burdens, and were selected as a representative sample of the wide variety of wastes currently generated. A clear dose response was observed for this parameter, with an increase in percentage of individual feeding inhibition with increased doses of organic wastes. More significantly, feeding inhibition correlated highly with mortality and reproduction inhibition in the different wastes. Composted sludges displayed the lowest toxicity, followed by thermally dried sludge and dewatered sludge. Thermally dried pig slurry showed the highest toxicity for feeding, with lower median effective concentration (EC50) values than the lowest dose tested. Among waste physicochemical parameters and pollutants, low organic matter stability appeared to be the main predictor of potential adverse effects on soil fauna, because it correlated significantly with feeding inhibition and mortality. Furthermore, feeding inhibition tests were run over a short exposure time (less than 7 d), which, together with the results obtained, makes this bioassay a good screening tool for organic waste toxicity.

Does lipophilicity of toxic compounds determine effects on drought tolerance of the soil collembolan Folsomia candida?

The ability of Collembola to survive drought stress is crucial for their distribution in the terrestrial environment. Previous studies have suggested that several toxic compounds affect the drought tolerance of Folsomia candida in a synergistic manner and that these compounds have the feature in common that they elicit their toxicity by causing membrane damage. We hypothesised that the detrimental effect of toxic chemicals on drought tolerance in F. candida depends on the lipophilicity (log K ow) of the compound because a higher log K ow would mean a closer interaction with membranes. In this study the three chemicals 4-nonylphenol, pyrene and p, p′-DDE were tested. Surprisingly, 4-nonylphenol, with the lowest log K ow, was the most potent with respect to reducing drought tolerance followed by pyrene, suggesting that interactions between drought tolerance and chemical stress do not depend on lipophilicity alone.

Effects of starvation and body mass on drought tolerance in the soil collembolan Folsomia candida

The effects of starvation and body mass on drought tolerance in Folsomia candida were investigated. Starvation for up to 6 weeks did not reduce tolerance to drought (98.2% RH) compared to a nonstarved control group. Animals starved for 1, 2 or 6 weeks prior to drought exposure showed no systematic differences in the accumulation of sugars and polyols (SP). In all groups exposed to drought SP constituted 9–13% of dry weight and was distributed in myoinositol, glucose and a third unidentified compound. At 97.3% RH large individuals (9 weeks old) survived better than small individuals (2 or 3 weeks old). However, no correlation was found between body mass and drought tolerance at relative humidities above 97.3% RH. The results suggest that starvation for ecologically relevant periods of time does not impair the ability to produce desiccation-protective SP in F. candida, and that both small and large life stages are well adapted to dry soil conditions.

Drought acclimation confers cold tolerance in the soil collembolan Folsomia candida

It has been noted that both summer drought and sub-zero winter temperatures induce the synthesis of sugars and polyols in invertebrate tissues. This has led several authors to suggest that many of the adaptations, previously viewed as a response to cold, might be part of a more universal desiccation tolerance mechanism. Here we show that acclimation of the soil dwelling collembolan Folsomia candida to a sublethal desiccation stress confers tolerance to cold shock and a significant increase in the molar percent of membrane fatty acids with a mid-chain double bond. These changes in membrane fatty acids are interpreted as conferring a significant reduction in the transition temperature of cell membranes, as would be expected in acclimation to cold, and these changes are therefore interpreted as contributing to the cross-tolerance. Drought acclimation was also shown to trigger the synthesis of the 70 kDa family of heat-shock proteins (Hsp70). This group of heat shock proteins is implicated in the reestablishment of the normal three-dimensional structure of partially unfolded proteins and therefore are also likely to contribute to the observed cross-tolerance. This study provides evidence that the stresses exerted by desiccation and cold at the cellular level have sufficient similarities to induce overlapping adaptations.