Comparative diversity of microbiomes and Resistomes in beef feedlots, downstream environments and urban sewage influent

Abstract

Background Comparative knowledge of microbiomes and resistomes across environmental interfaces between animal production systems and urban settings is lacking. In this study, we executed a comparative analysis of the microbiota and resistomes of metagenomes from cattle feces, catch basin water, manured agricultural soil and urban sewage. Results Metagenomic DNA from composite fecal samples (FC; n = 12) collected from penned cattle at four feedlots in Alberta, Canada, along with water from adjacent catchment basins (CB; n = 13), soil ( n = 4) from fields in the vicinity of one of the feedlots and urban sewage influent (SI; n = 6) from two municipalities were subjected to Illumina HiSeq2000 sequencing. Firmicutes exhibited the highest prevalence (40%) in FC, whereas Proteobacteria were most abundant in CB (64%), soil (60%) and SI (83%). Among sample types, SI had the highest diversity of antimicrobial resistance (AMR), and metal and biocide resistance (MBR) classes (13 & 15) followed by FC (10 & 8), CB (8 & 4), and soil (6 & 1). The highest antimicrobial resistant (AMR) gene (ARG) abundance was harboured by FC, whereas soil samples had a very small, but unique resistome which did not overlap with FC & CB resistomes. In the beef production system, tetracycline resistance predominated followed by macrolide resistance. The SI resistome harboured β-lactam, macrolide, tetracycline, aminoglycoside, fluoroquinolone and fosfomycin resistance determinants. Metal and biocide resistance accounted for 26% of the SI resistome with a predominance of mercury resistance. Conclusions This study demonstrates an increasing divergence in the nature of the microbiome and resistome as the distance from the feedlot increases. Consistent with antimicrobial use, tetracycline and macrolide resistance genes were predominant in the beef production system. One of the feedlots contributed both conventional (raised with antibiotics) and natural (raised without antibiotics) pens samples. Although natural pen samples exhibited a microbiota composition that was similar to samples from conventional pens, their resistome was less complex. Similarly, the SI resistome was indicative of drug classes used in humans and the greater abundance of mercury resistance may be associated with contamination of municipal water with household and industrial products. Electronic supplementary material The online version of this article (10.1186/s12866-019-1548-x) contains supplementary material, which is available to authorized users.

Insights Into the Resistome of Bovine Clinical Mastitis Microbiome, a Key Factor in Disease Complication

“…57 million kilograms of antibiotics are used annually in food animal production (Van Boeckel et al, 2015), which may select for antibiotic-resistant bacteria that persist throughout the meat and milk production chain. Investigation of the microbiome, and/or associated resistome of dairy animals especially in milk from cows with mastitis, and their environment may provide valuable data and models to estimate the public health risk of antibiotic-resistant human infections associated with antibiotic use in dairy animals (Zaheer et al, 2019). Our present findings are sufficiently enriched in taxonomic resolution and predicted protein functions, and corroborates the findings of several previous studies (Oikonomou et al, 2014;Falentin et al, 2016;Patel et al, 2017;Hoque et al, 2019).…”

“…The vast diversity of bacterial species in CM milk, many with short generation times and rampant horizontal gene transfer, permit the rapid accumulation of countless resistant variants at a relatively high evolutionary pace (D'Costa et al, 2011;Weller and Wu, 2015). However, resistance in CM bacteria typically goes unnoticed until a given species becomes of clinical interest, and the associated resistome is also suspected to be a source of newly emerging resistance genes in CM pathogens (Krömker and Leimbach, 2017;Cheng et al, 2019;Hoque et al, 2019;Zaheer et al, 2019). Bacteria residing in the bovine gastrointestinal tract and udder may become resistant to these antibiotics and, once released into the milk, they may take part in horizontal transfer of antibiotic resistance genes (ARGs) to other CM bacteria of contagious and environmental origin (Cheng et al, 2019;Zaheer et al, 2019).…”

“…However, resistance in CM bacteria typically goes unnoticed until a given species becomes of clinical interest, and the associated resistome is also suspected to be a source of newly emerging resistance genes in CM pathogens (Krömker and Leimbach, 2017;Cheng et al, 2019;Hoque et al, 2019;Zaheer et al, 2019). Bacteria residing in the bovine gastrointestinal tract and udder may become resistant to these antibiotics and, once released into the milk, they may take part in horizontal transfer of antibiotic resistance genes (ARGs) to other CM bacteria of contagious and environmental origin (Cheng et al, 2019;Zaheer et al, 2019). Furthermore, AMR is a global health concern in both human and veterinary medicine (Van Boeckel et al, 2015), and thus, monitoring the emergence of AMR strains is an essential component of bovine CM prevention and control strategies (Tomazi et al, 2018;Cheng et al, 2019).…”

Host genetics affected the resistome and its expression patterns in the rumen of beef cattle raised without antibiotics used in humans

“…In this study, metagenomic analysis revealed that the abundance of ARGs in the rumen of beef steers were predominant by tetracycline (77%) and followed by MLS (17%), and aminoglycoside (4%) resistance. These ndings are similar to those reported in fecal samples of beef cattle fed with antibiotics (ionophores, chlortetracycline, or tylosin), where tetracycline resistance was most prevalent (82%), followed by macrolide (14%), and aminoglycoside [32]). In addition, tetracycline, MLS, and aminoglycoside classes of resistance were also predominant in fecal samples of feedlot cattle raised without antibiotic [33], suggesting that the pro les of ARG are consistent in different locations of digestive tract of ruminants.…”

Surveillance of Enterococcus spp. reveals distinct species and antimicrobial resistance diversity across a One-Health continuum

“…1A) were sampled for two consecutive years (March 2014 -April 2016). As previously described 79 , production conditions were typical for western Canadian commercial cattle feedlots, with animals housed in open-air, dirt-floor pens arranged side-by-side with central feed alleys. Fecal sampling was conducted according to a protocol approved by the Animal Care Committee, University of Calgary (Protocol ID: AC14-0029).…”