Gene exchange drives the ecological success of a multi-host bacterial pathogen

Abstract

The capacity for some pathogens to jump into different host-species populations is a major threat to public health and food security. Staphylococcus aureus is a multi-host bacterial pathogen responsible for important human and livestock diseases. Here, using a population-genomic approach, we identify humans as a major hub for ancient and recent S. aureus host-switching events linked to the emergence of endemic livestock strains, and cows as the main animal reservoir for the emergence of human epidemic clones. Such host-species transitions are associated with horizontal acquisition of genetic elements from host-specific gene pools conferring traits required for survival in the new host-niche. Importantly, genes associated with antimicrobial resistance are unevenly distributed among human and animal hosts, reflecting distinct antibiotic usage practices in medicine and agriculture. In addition to gene acquisition, genetic diversification has occurred in pathways associated with nutrient acquisition, implying metabolic remodelling after a host switch in response to distinct nutrient availability. For example, S. aureus from dairy cattle exhibit enhanced utilization of lactose-a major source of carbohydrate in bovine milk. Overall, our findings highlight the influence of human activities on the multi-host ecology of a major bacterial pathogen, underpinned by horizontal gene transfer and core genome diversification.

Gene loss and acquisition in lineages of bacteria evolving in a human host environment

“…The study used genomic data from a previously reported collection of 474 clinical isolates of P. aeruginosa that were sampled from 34 patients with CF attending the Copenhagen Cystic Fibrosis Center at the University Hospital, Rigshospitalet, Denmark [10]. Genomes were sequenced as follows: genomic DNA was prepared from P. aeruginosa isolates on a QIAcube system using a DNeasy Blood and Tissue kit (Qiagen) and sequenced on an Illumina HiSeq 2000 platform, generating 100-bp paired-end reads and using a multiplexed protocol to obtain an average of 7,139,922 reads (range of 3,111,085,190) for each of the genomic libraries.…”

“…[1,2] In contrast to point mutations, small insertions and deletions (microindels), inversions, and translocations that gradually alter existing genomic content, the acquisition or loss of entire genes rapidly confers large changes to the genomic content, and gene acquisition and loss alters phenotypes such as virulence, antibiotic resistance, and metabolic capability. [3,4] Thus, genome-wide analysis of the gene presence or absence is necessary to better understand the bacterial evolution and adaptation.…”

Molecular Epidemiology of Methicillin-Susceptible and Methicillin-Resistant Staphylococcus aureus in Wild, Captive and Laboratory Rats: Effect of Habitat on the Nasal S. aureus Population

“…The core variable genome contains the information for surface proteins and transcription regulators, while the accessory genome consists mainly of mobile genetic elements (MGEs), and thus represents the most variable part of the genome [27][28][29]. Unsurprisingly, the accessory genome plays a major role in adaptation processes of S. aureus [30], allowing it to adapt to changing environments, such as different host species. Prominent examples include: (i) lack of antibiotic resistance genes and the highly human-specific immune evasion gene cluster (IEC) in animal isolates; (ii) lack of superantigen genes in murine S. aureus isolates; (iii) acquisition of variants of the von Willebrand factor-binding protein in ruminant and equine strains, carried by highly mobile pathogenicity islands (SaPIs); as well as (iv) a single nucleotide mutation in the dltB gene, a gene involved in lipoteichoic acid biosynthesis, which enabled a human strain to infect rabbits [10,11,[31][32][33][34].…”

Genomes of a major nosocomial pathogenEnterococcus faeciumare shaped by adaptive evolution of the chromosome and plasmidome

“…1A, https://microreact.org/project/BJKGTJPTQ), they only covered a fraction of the full genome (978 orthologous groups). Analyses of accessory genes can provide a more compelling picture of the evolution of a species, for example by revealing niche-specific signals that represent the adaptation of different clones to similar environments (Richardson et al 2018). The pan-genome of the 1,644 E. faecium isolates was composed of 30,855 orthologous groups and it was used to visualize isolate relatedness based on shared gene content analysis using PANINI ( Fig.…”