The honeybee gut resistome and its role in antibiotic resistance dissemination

Sun, Hongtao; Li, Hu; Zhang, Xue; Liu, Yan; Chen, Hao; Zheng, Li; Zhai, Yifan; Zheng, Hao

doi:10.1111/1749-4877.12714

Cited by 9 publications

(5 citation statements)

References 116 publications

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“…Cockroaches harbor a diverse gut microbiome, more diverse than that of the common animal model D. melanogaster ( 52 ), yet not as complex as cockroaches’ close relatives, the eusocial termites ( 20 , 53 ). Other eusocial insects, in particular the honey bee Apis mellifera , carry ARGs ( 54 ) and have also been used as experimental models in microbiome research ( 55 ). However, the rearing and maintenance of eusocial insect colonies require specialist knowledge ( 56 ), while the rigidly structured inter-individual interactions may complicate the dynamics of transmission studies.…”

Section: Discussionmentioning

confidence: 99%

Transmission of antimicrobial resistance in the gut microbiome of gregarious cockroaches: the importance of interaction between antibiotic exposed and non-exposed populations

Bogri,

Jensen,

Borchert

et al. 2024

mSystems

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Antimicrobial resistance (AMR) is a major global health concern, further complicated by its spread via the microbiome bacterial members. While mathematical models discuss AMR transmission through the symbiotic microbiome, experimental studies are scarce. Herein, we used a gregarious cockroach, Pycnoscelus surinamensis, as an in vivo animal model for AMR transmission investigations. We explored whether the effect of antimicrobial treatment is detectable with metagenomic sequencing, and whether AMR genes can be spread and established in unchallenged (not treated with antibiotics) individuals following contact with treated donors, and under various frequencies of interaction. Gut and soil substrate microbiomes were investigated by metagenomic sequencing for bacterial community composition and resistome profiling. We found that tetracycline treatment altered the treated gut microbiome by decreasing bacterial diversity and increasing the abundance of tetracycline resistance genes. Untreated cockroaches that interacted with treated donors also had elevated tetracycline resistance. The levels of resistance differed depending on the magnitude and frequency of donor transfer. Additionally, treated donors showed signs of microbiome recovery due to their interaction with the untreated ones. Similar patterns were also recorded in the soil substrate microbiomes. Our results shed light on how interacting microbiomes facilitate AMR gene transmission to previously unchallenged hosts, a dynamic influenced by the interaction frequencies, using an in vivo model to validate theoretical AMR transmission models. IMPORTANCE Antimicrobial resistance is a rising threat to human and animal health. The spread of resistance through the transmission of the symbiotic gut microbiome is of concern and has been explored in theoretical modeling studies. In this study, we employ gregarious insect populations to examine the emergence and transmission of antimicrobial resistance in vivo and validate modeling hypotheses. We find that antimicrobial treatment increases the levels of resistance in treated populations. Most importantly, we show that resistance increased in untreated populations after interacting with the treated ones. The level of resistance transmission was affected by the magnitude and frequency of population mixing. Our results highlight the importance of microbial transmission in the spread of antimicrobial resistance.

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Section: Discussionmentioning

confidence: 99%

Transmission of antimicrobial resistance in the gut microbiome of gregarious cockroaches: the importance of interaction between antibiotic exposed and non-exposed populations

Bogri,

Jensen,

Borchert

et al. 2024

mSystems

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“…There are also some research has shown that by high-fat lowcarbohydrate diet, reduce body fat, reach the purpose of reducing weight, reduce the probability of the metabolic syndrome, thus reducing insulin resistance, achieve the goal of control blood glucose levels. [9]…”

Section: The Relationship Between High-fat Low-carbohydrate Diet and ...mentioning

confidence: 99%

Effect of High-fat Low-carbohydrate Diet on the Structure of Intestinal Flora in T2DM Patients: A Narrative Review

Zhang

2023

IJBLS

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High-fat low-carbohydrate diets are currently popular as one of the methods of weight loss, and the influence of this diet on the structure of intestinal flora in T2DM is a topical issue in the field of research. Despite the controversial result of the studies published so far in patients with type 2 diabetes. As one of the important microbial symbiotic systems in the human body, the intestinal flora is considered to be closely related to the development of type 2 diabetes. The intestinal flora structure abundance of type 2 diabetes patients is different from that of the general healthy population, and alterations in the structure of the intestinal flora can affect intestinal hormone secretion, which in turn affects the blood glucose level in type 2 diabetic patients. It is feasible to treat type 2 diabetes by altering the intestinal flora. Therefore, this narrative review proposes that the possible reason for the treatment of T2DM by high-fat low-carbohydrate diet is that the method of high-fat low-carbohydrate diet alters the intestinal flora structure of patients with T2DM, and treats patients with T2DM by altering their intestinal flora structure, which provides some new ideas and methods for the treatment and prevention of T2DM.

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“…EFB control is based on applying broad-spectrum antibiotics that are authorized for treating honey bees [ 10 , 11 , 12 ]. Among those, oxytetracycline (OTC)-containing products are the most widespread in beekeeping for controlling various bacterial honey bee diseases, resulting in increasing rates of antibiotic resistance (ABR) [ 5 , 10 , 13 ].…”

Section: Introductionmentioning

confidence: 99%

“…Genes coding ABR against OTC can also spread horizontally via mobile genetic elements (e.g., plasmids or transposons). On a host population level, such bacteria can be transmitted by social behavior and the environment [ 12 ].…”

Section: Introductionmentioning

confidence: 99%

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IPM Strategy to Control EFB in Apis mellifera: Oxytetracycline Treatment Combined with Partial Shook Swarm and Queen Caging

Mosca,

Gyorffy,

Pietropaoli

et al. 2024

Veterinary Sciences

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We tested an integrated pest management (IPM) strategy to control European foulbrood (EFB) in honey bees. Colonies affected by EFB were assigned to two homogenous groups: an oxytetracycline-treated group (1.5 g OTC/hive) that underwent partial shook swarm (PSS) in combination with queen caging (QC) and an untreated group where only two beekeeping techniques, PSS and QC, were applied. The consumption of sucrose solution, the strength of the colonies, side effects of the mentioned techniques, clinical as well as subclinical relapses of EFB, and the amount of OTC residues in the honey were assessed over a 7-month-long monitoring period. Regarding the consumption of the sucrose solution, there was no significant difference between the OTC-treated and untreated groups. The strength of the untreated colonies was consistently but not significantly higher than those treated with OTC. PSS combined with QC resulted in various side effects in both groups: queen loss (52%), absconding (8%), and drone-laying queen (4%). Untreated colonies (16.7%) showed clinical EFB relapses 4 months after the application of PSS along with QC, while 15.4% of the OTC-treated colonies were confirmed EFB-positive by PCR. OTC residues were detected in the honey yielded in the cases of both groups. Two months after the PSS, the amount of OTC residues in the untreated group was 0.6 ± 0.2 µg/kg, while that in the OTC-treated group amounted to 5.8 ± 11.6 µg/kg; both results are below the maximum residue limit (MRL) of 100 ppb considered in the EU for cascade use.

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The honeybee gut resistome and its role in antibiotic resistance dissemination

Cited by 9 publications

References 116 publications

Transmission of antimicrobial resistance in the gut microbiome of gregarious cockroaches: the importance of interaction between antibiotic exposed and non-exposed populations

Transmission of antimicrobial resistance in the gut microbiome of gregarious cockroaches: the importance of interaction between antibiotic exposed and non-exposed populations

Effect of High-fat Low-carbohydrate Diet on the Structure of Intestinal Flora in T2DM Patients: A Narrative Review

IPM Strategy to Control EFB in Apis mellifera: Oxytetracycline Treatment Combined with Partial Shook Swarm and Queen Caging

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