Invasive Streptococcus suis isolated in Spain contain a highly promiscuous and dynamic resistome
Cristina Uruén1,2, Jorge Gimeno1,2, Marina Sanz1,2
1Unit of Microbiology and Immunology, Faculty of Veterinary, University of Zaragoza, Zaragoza, Spain.
Introduction:
Streptococcus suis is a major pathogen for swine and human. Here we aimed to know the rates of antimicrobial resistance (AMR) in invasive S. suis isolates recovered along Spain between 2016 - 2021 and elucidate their genetic origin.
Methods:
Antibiotic susceptibility testing was performed for 116 isolates of different genetic backgrounds and geographic origins against 18 antibiotics of 9 families. The association between AMR and genotypes and the origin of the isolates were statistically analyzed using Pearson´s chi-square test and the likelihood ratio. The antimicrobial resistant genes were identified by whole genome sequencing analysis and PCR screenings.
Results:
High AMR rates (>80%) were detected for tetracyclines, spectinomycin, lincosamides, and marbofloxacin, medium (20-40%) for sulphonamides/trimethoprim, tiamulin, penicillin G, and enrofloxacin, and low (< 20%) for florfenicol, and four additional β-lactams. The occurrence of multidrug resistance was observed in 90% of isolates. For certain antibiotics (penicillin G, enrofloxacin, marbofloxacin, tilmicosin, and erythromycin), AMR was significantly associated with particular sequence types (STs), geographic regions, age of pigs, and time course. Whole genome sequencing comparisons and PCR screenings identified 23 AMR genes, of which 19 were previously reported in S. suis (aph(3')-IIIa, sat4, aadE, spw, aac(6')-Ie-aph(2'')-Ia, fexA, optrA, erm(B), mef(A/E), mrs(D), mph(C), lnu(B), lsa(E), vga(F), tet(M), tet(O), tet(O/W/32/O), tet(W)), and 4 were novel (aph(2'')-IIIa, apmA, erm(47), tet(T)). These AMR genes explained the AMR to spectinomycin, macrolides, lincosamides, tiamulin, and tetracyclines. Several genes were located on mobile genetic elements which showed a variable organization and composition. As AMR gene homologs were identified in many human and animal pathogens, the resistome of S. suis has a different phylogenetic origin. Moreover, AMR to penicillin G, fluoroquinolones, and trimethoprim related to mutations in genes coding for target enzymes (pbp1a, pbp2b, pbp2x, mraY, gyrA, parC, and dhfr). Bioinformatic analysis estimated traits of recombination on target genes, also indicative of gene transfer events.
Conclusions:
Our work evidences that S. suis is a major contributor to AMR dissemination across veterinary and human pathogens. Therefore, control of AMR in S. suis should be considered from a One Health approach in regions with high pig production to properly tackle the issue of antimicrobial drug resistance.
Insights
Antimicrobial resistance (AMR) is high in Streptococcus suis, a swine and human pathogen. Genetic analysis revealed specific AMR genes and mutations, highlighting the need for a One Health approach to control AMR spread.
Area of Science:
- Veterinary Microbiology
- Antimicrobial Resistance
- One Health
Background:
- Streptococcus suis is a significant pathogen affecting both swine and human health.
- Understanding antimicrobial resistance (AMR) patterns in S. suis is crucial for public and animal health.
- Surveillance of AMR in S. suis is essential, particularly in regions with intensive pig farming.
Purpose of the Study:
- To determine the rates of AMR in invasive S. suis isolates in Spain from 2016 to 2021.
- To investigate the genetic origins and mechanisms of AMR in these isolates.
- To assess the potential for AMR dissemination between animal and human pathogens.
Main Methods:
- Antibiotic susceptibility testing was performed on 116 S. suis isolates against 18 antibiotics.
- Statistical analysis was used to associate AMR with isolate genotypes and origins.
- Whole genome sequencing and PCR screening identified antimicrobial resistance genes and mutations.
Main Results:
- High AMR rates (>80%) were observed for tetracyclines, spectinomycin, lincosamides, and marbofloxacin.
- Multidrug resistance was prevalent, found in 90% of isolates.
- 23 AMR genes were identified, including 4 novel ones, with several located on mobile genetic elements. Mutations in target genes also contributed to resistance.
Conclusions:
- S. suis plays a significant role in the dissemination of AMR among veterinary and human pathogens.
- Control of AMR in S. suis requires a One Health approach, integrating animal and human health strategies.
- Effective AMR management in S. suis is vital for regions with high pig production to mitigate public health risks.
