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Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish.

ABSTRACT: Prophylactic antibiotics in the aquaculture and ornamental fish industry are intended to prevent the negative impacts of disease outbreaks. Research in mice and humans suggests that antibiotics may disturb microbiome communities and decrease microbiome-mediated disease resistance, also known as "colonization resistance." If antibiotics impact fish as they do mice and humans, prophylactic administrations on aquaculture farms may increase downstream disease susceptibility in target hosts, despite short-term pathogen control benefits. We tested the effects of antibiotics on mortality after a pathogen challenge in the Poecilia sphenops black molly and subsequently tested if probiotic inoculations could reverse any antibiotic-induced losses of disease resistance. We found that antibiotic treatment significantly increased fish mortality. We further found that our two candidate probiotic bacterial species, Phaeobacter inhibens S4Sm and Bacillus pumilus RI06-95Sm, were able to colonize black molly microbiomes and reverse the negative impacts of antibiotics. Despite the positive impact on survival, probiotic treatment did not influence overall microbiome community structure or diversity. Our results suggest that subtle manipulations of microbiome composition can have dramatic impacts on host phenotype. The results of this study have implications for how antibiotic-treated microbiomes can be restored and suggest that small-scale additions may be as effective as wholesale transplants. IMPORTANCE Prophylactic antibiotics are widespread in the aquaculture industry and are used where vaccination is impossible or overly expensive. If antibiotics impact fish as they do mice and humans, prophylactic administrations in aquaculture and ornamental fish farms may increase downstream disease susceptibility in target hosts, despite short-term pathogen control benefits. Recent research has suggested that their use exacerbates bacterial outbreaks by creating sterile, nutrient-rich environments for invading pathogens to colonize and could help to explain rising economic costs of bacterial outbreaks in aquaculture. Our findings suggest a long-term cost of prophylactic antibiotic use and demonstrate a probiotic-based solution that does not rely on full microbiome community transplantation.

SUBMITTER: Schmidt V

PROVIDER: S-EPMC5675916 | biostudies-literature | 2017 Nov-Dec

REPOSITORIES: biostudies-literature

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Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish.

Schmidt Victor V Gomez-Chiarri Marta M Roy Chelsea C Smith Katherine K Amaral-Zettler Linda L

mSystems 20171107 6

Prophylactic antibiotics in the aquaculture and ornamental fish industry are intended to prevent the negative impacts of disease outbreaks. Research in mice and humans suggests that antibiotics may disturb microbiome communities and decrease microbiome-mediated disease resistance, also known as "colonization resistance." If antibiotics impact fish as they do mice and humans, prophylactic administrations on aquaculture farms may increase downstream disease susceptibility in target hosts, despite ...[more]

PMID: 29124129

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Project description:AimAntibiotic-associated diarrhea (AAD) is a common side effect during antibiotic treatment, which can cause dysbacteriosis of the gut microbiota. Previous studies have shown beneficial effects in AAD treatment with Bifidobacterium lactis XLTG11, Lactobacillus casei Zhang, Lactobacillus plantarum CCFM8661, and Lactobacillus rhamnosus Probio-M9. However, no studies have been conducted on the immunomodulatory effects and protective intestinal barrier function of four complex probiotics. The aim of our study is to investigate the alleviation effects of complex probiotics on ampicillin-induced AAD.MethodsThirty-six BALB/c mice were randomly divided into six groups: normal control group (NC), model control group (MC), low-, medium-, and high-dose probiotics groups (LD, MD, and HD), and positive drug (Bifico, 1 × 107 cfu) control group (PDC; Bifico, also known as Bifidobacterium Triple Live Capsule, is composed of Bifidobacterium longum, Lactobacillus acidophilus, and Enterococcus faecalis). An AAD model was established by intragastric administration of ampicillin, by gavage of different doses of complex probiotics and Bifico. The weight gain, fecal water content, loose stool grade, intestinal permeability, total protein and albumin levels, intestinal barrier, cytokine levels, and gut microbiota were determined.ResultsThe results showed that complex probiotics significantly decreased the fecal water content, loose stool grade, intestinal permeability, and ileum tissue damage. Their application increased the weight gain, SIgA, TP, and ALB levels. Additionally, complex probiotics significantly decreased the levels of pro-inflammatory cytokines and increased those of anti-inflammatory cytokines. Meanwhile, the mRNA expression levels of ZO-1, occludin, claudin-1, and MUC2 were significantly upregulated in the probiotic-treated group. Furthermore, the complex probiotics increased the gut microbiota diversity and modulated the changes in the gut microbiota composition caused by ampicillin. At the phylum level, the abundance of Proteobacteria in the HD group was lower than that in the MC group, whereas that of Bacteroidetes was higher. At the genus level, the abundances of Klebsiella and Parabacteroides in the HD group were lower, whereas those of Bacteroides, Muribaculaceae, and Lactobacillus were higher than those in the MC group. Moreover, Spearman's correlation analysis also found that several specific gut microbiota were significantly correlated with AAD-related indicators.ConclusionWe found that complex probiotics improved the diarrhea-related indexes, regulated gut microbiota composition and diversity, increased the expression levels of intestinal protective barrier-related genes, preserved the intestinal barrier function, and relieved inflammation and intestinal injury, thereby effectively improving AAD-associated symptoms. Graphical Abstract.

Project description:Background:Antibiotic-resistant (AR) bacteria are a global threat. AR bacteria can be acquired in early life and have long-term sequelae. Limiting the spread of antibiotic resistance without triggering the development of additional resistance mechanisms is of immense clinical value. Here, we show how the infant gut microbiome can be modified, resulting in a significant reduction of AR genes (ARGs) and the potentially pathogenic bacteria that harbor them. Methods:The gut microbiome was characterized using shotgun metagenomics of fecal samples from two groups of healthy, term breastfed infants. One group was fed B. infantis EVC001 in addition to receiving lactation support (n?=?29, EVC001-fed), while the other received lactation support alone (n?=?31, controls). Coliforms were isolated from fecal samples and genome sequenced, as well as tested for minimal inhibitory concentrations against clinically relevant antibiotics. Results:Infants fed B. infantis EVC001 exhibited a change to the gut microbiome, resulting in a 90% lower level of ARGs compared to controls. ARGs that differed significantly between groups were predicted to confer resistance to beta lactams, fluoroquinolones, or multiple drug classes, the majority of which belonged to Escherichia, Clostridium, and Staphylococcus. Minimal inhibitory concentration assays confirmed the resistance phenotypes among isolates with these genes. Notably, we found extended-spectrum beta lactamases among healthy, vaginally delivered breastfed infants who had never been exposed to antibiotics. Conclusions:Colonization of the gut of breastfed infants by a single strain of B. longum subsp. infantis had a profound impact on the fecal metagenome, including a reduction in ARGs. This highlights the importance of developing novel approaches to limit the spread of these genes among clinically relevant bacteria. Future studies are needed to determine whether colonization with B. infantis EVC001 decreases the incidence of AR infections in breastfed infants. Trial registration:This clinical trial was registered at ClinicalTrials.gov, NCT02457338.

Project description:BACKGROUND:Antibiotic-associated diarrhea (AAD) occurs in 2-25% of nursing home residents, which may lead to dehydration, malnutrition, severe complications and hospitalizations. Research shows that probiotics can be effective and safe in reducing AAD. However, probiotics are not routinely used in Dutch nursing homes. The objectives of this evaluation were to develop a procedure for the implementation of probiotics to prevent AAD in nursing homes, to evaluate effects on AAD occurrence, and to evaluate the implementation process of probiotics in daily care. METHODS:A pragmatic participatory evaluation (PPE) design was chosen, as it seemed a suitable approach for implementation of probiotics, as well as for evaluation of its effectiveness in daily nursing home practice. Probiotics administration was implemented in three nursing homes of the Rivas Zorggroep for residents with somatic and/or psychogeriatric conditions. Ninety-three residents provided data on 167 episodes of antibiotics use, of which 84 episodes that included supplementation with probiotics and 83 episodes with no probiotics supplementation. A multispecies probiotics was administered twice daily upon start of antibiotic treatment, up to 1?week after completing the antibiotics course. The occurrence of AAD was monitored and a process evaluation was conducted to assess facilitators and barriers of probiotics implementation. RESULTS:The number of episodes with AAD when using probiotics was significantly lower than when no probiotics was used (20% vs 36%; p?=?0,022, Chi-square). No significant differences in the occurrence of AAD were found between the residents taking amoxicillin/clavulanic acid or ciprofloxacin. Reported facilitators for implementation were perceived benefits of probiotics and prescription by medical staff. Reported challenges were probiotics intake by residents and individual decision-making as to which resident would benefit from it. CONCLUSION:Successful implementation of probiotics demonstrated the prevention of AAD in nursing home residents. TRIAL REGISTRATION:ISRCTN 94786163, retrospectively registered on 3 February 2020.

Project description:Aquaculture is a fast-growing animal food sector, and freshwater fish farming is particularly common in Central and Eastern Europe. As the biodiversity of fishery ponds is changed toward fulfilling the industrial needs, precautions should be taken to keep the system sustainable and protect the adjacent environment from possible damage. Due to risk of infectious diseases, antibiotics are used in aquaculture production systems. The constant exposure to antimicrobials can contribute to the rise of antibiotic resistance in aquaculture products and the adjacent ecosystems, with possibility of dissemination to the wider environment as well as between animals and humans. Even though previous studies have found antibiotic resistance genes in the sediments and water of farming ponds, the tendency and direction of spreading is not clear yet. The objective of this project was to evaluate the influence of intensive fish farming on the condition of water bodies used for the aquaculture and the environment, concentrating on the impact of the aquaculture on the surrounding water ecosystems as well as the possibility of transferring the pollutants and antibiotic resistance genes to both environment and the human hosts. Combined measurement of antibiotic and heavy metal contamination, toxicity assessment, microorganism diversity, and the detection of common antibiotic resistance genes was performed in the sediments of one fishery farm ponds as well as sampling points upstream and downstream. All the tested sediment samples did not show significantly elevated heavy metal concentrations and no substantial veterinary antibiotic pollution. From the antibiotic resistance genes tested, the presence of aminoglycoside and β-lactam resistance determinants as well as the presence of integrons could be of concern for the possibility of transfer to humans. However, despite the lack of heavy metal and antibiotic pollution, the sediments showed toxicity, the cause of which should be explored more.

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Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish.

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Subtle Microbiome Manipulation Using Probiotics Reduces Antibiotic-Associated Mortality in Fish.

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