Prospective comparison of the digestive tract resistome and microbiota in cattle raised in grass-fed versus grain-fed production systems.

IF 3.7 2区 生物学 Q2 MICROBIOLOGY
mSphere Pub Date : 2025-03-25 Epub Date: 2025-02-14 DOI:10.1128/msphere.00738-24
Jiye Kwon, Windy Tanner, Yong Kong, Martina Wade, Chad Bitler, Marilia B Chiavegato, Melinda M Pettigrew
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引用次数: 0

Abstract

Most antimicrobials sold in the United States are used in food animals. Farm management practices contribute to antibacterial resistance (AR). Controversially, grass-fed diets have been recommended over grain-fed diets to reduce AR in beef cattle. Ionophore feed additives (non-therapeutic antibiotics that enhance feed efficiency) may contribute to AR development. We used shotgun metagenomic sequencing of fecal swabs to prospectively compare the cattle gastrointestinal resistome and microbiota in two different production systems over five periods from pre-weaning to pre-harvest. Cattle were grass-fed and pasture-raised (system A, n = 33) or grain-fed with ionophore additives in feedlots (system B, n = 34). System A cattle averaged 639 lb and 22.8 months of age, and system B cattle averaged 1,173 lb and 12.4 months of age preharvest. In total, 367 antibiotic resistance genes (ARGs) and 329 bacterial species were identified. The resistome of system A cattle had higher alpha diversity than system B cattle over their lifespan (P = 0.008). Beta-diversity estimates indicated overlap in the pre-weaning resistome and microbiota in both systems, which diverged post-weaning, with increases in several medically important ARGs when system B cattle transitioned to a grain diet. Analysis of compositions of microbiomes with bias correction indicated that levels of tetracycline, macrolide, aminoglycoside, beta-lactam, and bacitracin ARGs were significantly higher in system B cattle pre-harvest. Resistome changes were highly correlated with bacterial community changes (Procrustes, M2 = 0.958; P = 0.001). Potentially modifiable farm management strategies, including diet and ionophores, may influence abundance and diversity of ARGs in fecal samples from cattle.IMPORTANCEAntibiotic resistance is a One Health threat. More antibiotics are used in agriculture than in human medicine. We compared the relative abundance of antibiotic resistance genes (ARGs) and bacterial species in cattle raised in two different cattle production systems (grass- and grain-fed). Fecal swab samples were collected at five time points spanning pre-weaning and prior to harvest. The antibiotic resistance gene and bacterial communities were relatively similar in the pre-weaning period when cattle in both systems were milking and on pasture. Resistance genes and bacterial communities diverged post-weaning when system B cattle were given a grain diet with feed additives for growth promotion containing non-medically important antibiotics (i.e., ionophores). The levels of medically important ARGs (e.g., macrolides) increased in system B grain-fed cattle post-weaning and were higher than in system A just prior to slaughter. These data provide additional evidence that farm management strategies impact the level of antibiotic resistance.

草饲和谷物饲牛消化道抵抗组和微生物群的前瞻性比较。
在美国销售的大多数抗菌剂都用于食用动物。农场管理做法有助于抗菌药物耐药性(AR)。有争议的是,为了减少肉牛的反刍反应,草饲饲料比谷物饲料更被推荐。离子载体饲料添加剂(提高饲料效率的非治疗性抗生素)可能有助于AR的发展。我们使用鸟枪宏基因组测序法对粪拭子进行前瞻性比较,从断奶前到收获前的五个时期,两种不同生产系统中的牛胃肠道抵抗组和微生物群。采用草饲和牧场饲养(系统A, n = 33)或在饲养场中添加离子载体添加剂的谷物饲养(系统B, n = 34)。A系统牛收获前平均体重639磅,月龄22.8个月,B系统牛收获前平均体重1173磅,月龄12.4个月。共鉴定出367个抗生素耐药基因(ARGs)和329种细菌。系统A牛的α多样性高于系统B牛(P = 0.008)。β -多样性估计表明,断奶前两种系统的抗性组和微生物群存在重叠,断奶后出现分化,当系统B牛过渡到谷物日粮时,几种医学上重要的ARGs增加。偏倚校正后的微生物组组成分析表明,收获前B系统牛的四环素、大环内酯、氨基糖苷、β -内酰胺和杆菌肽ARGs水平显著较高。抵抗组变化与细菌群落变化高度相关(Procrustes, M2 = 0.958;P = 0.001)。可能改变的农场管理策略,包括饮食和离子载体,可能会影响牛粪便样本中ARGs的丰度和多样性。抗生素耐药性是一种健康威胁。抗生素在农业上的使用比在人类医学上的使用要多。我们比较了在两种不同的牛生产系统(草饲和谷物饲)中饲养的牛的抗生素抗性基因(ARGs)和细菌种类的相对丰度。在断奶前和收获前的五个时间点收集粪便拭子样本。两种系统的牛在断奶前挤奶和放牧期间的抗生素抗性基因和细菌群落相对相似。断奶后给B系统牛饲喂含有非医学上重要抗生素(即离子载体)促进生长的饲料添加剂的谷物饲粮时,抗性基因和细菌群落出现分化。B系统谷物饲养的牛在断奶后具有重要医学意义的ARGs(如大环内酯类)水平增加,在屠宰前高于A系统。这些数据为农场管理策略影响抗生素耐药性水平提供了额外证据。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
mSphere
mSphere Immunology and Microbiology-Microbiology
CiteScore
8.50
自引率
2.10%
发文量
192
审稿时长
11 weeks
期刊介绍: mSphere™ is a multi-disciplinary open-access journal that will focus on rapid publication of fundamental contributions to our understanding of microbiology. Its scope will reflect the immense range of fields within the microbial sciences, creating new opportunities for researchers to share findings that are transforming our understanding of human health and disease, ecosystems, neuroscience, agriculture, energy production, climate change, evolution, biogeochemical cycling, and food and drug production. Submissions will be encouraged of all high-quality work that makes fundamental contributions to our understanding of microbiology. mSphere™ will provide streamlined decisions, while carrying on ASM''s tradition for rigorous peer review.
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