Prophages and adaptation of Staphylococcus aureus ST398 to the human clinic

Abstract

BackgroundIt has been suggested that prophages in the ST398 S. aureus clone are responsible for expanding ST398's spectrum of action and increasing its ability to cause human infections. We carried out the first characterization of the various prophages carried by 76 ST398 bloodstream infection (BSI) isolates obtained over 9 years of observation.ResultsWhole-genome sequencing of 22 representative isolates showed (1) the presence of the φ3-prophage and diverse genetic features typical of animal-associated isolates (i.e., SCCmec XI element, Tn916 transposon and non φ3-prophages) in a majority of BSI isolates, (2) one BSI isolate devoid of the φ3-prophage but otherwise similar to an animal-infecting isolate, (3) 35 prophages carrying numerous genes previously associated with virulence or immune evasion in animal models of staphylococcal infections. The analysis of prophage content in all 76 BSI isolates showed an increasing prevalence of polylysogeny over time. Overall, over the course of the last 10 years, the BSI isolates appear to have acquired increasing numbers of genetic features previously shown to contribute to bacterial adaptation and virulence in animal models of staphylococcal infections.ConclusionsWe hypothesize that lysogeny has played a significant role in increasing the ability of the ST398 clone to cause infections in humans. Our findings highlight the risk that the ST398 lineage will increase its threat to public health by continuing to acquire virulence and/or multiple antibiotic-resistance genes from hospital-associated clones of Staphylococcus aureus.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3516-x) contains supplementary material, which is available to authorized users.

Antimicrobial Resistance and Molecular Epidemiology of Staphylococcus aureus Causing Bloodstream Infections at Ruijin Hospital in Shanghai from 2013 to 2018

“…More recently, CC398 MSSA have been increasingly being reported as the cause of invasive infections among patients who have no contact with livestock, and CC398 MSSA bloodstream infections were always associated with high mortality 34 . It has been hypothesized that lysogeny may play an important role in increasing the ability of ST398 clone to cause human infections, and the significant risk calling for urgent attention is that ST398 clone family will still increase its threat to public health by continuing to obtain virulence and/or multidrug resistance genes from healthcare-associated S. aureus clones 35 . Therefore, it is deeply needed to monitor the extraordinary cloning of human adaptive S. aureus like CC398 and genomic studies might can figure out the determinants of its diffusion.…”

Prevalence and Genomic Structure of Bacteriophage phi3 in Human-Derived Livestock-Associated Methicillin-Resistant Staphylococcus aureus Isolates from 2000 to 2015

“…Until now, human-adapted MSSA CC398 isolates harboring the phi3 phage were mainly assigned to spa types t571, t034, and t3625 and were associated with human infections (16,18,31,44,45). Furthermore, bacteriophage phi3 was found in MSSA CC398 isolates belonging to the spa types t899, t571, t1451, t5635, t6587, and t9378 obtained from bloodstream infections in France (14). In Spain, an MRSA CC398 isolate containing bacteriophage phi3 belonging to spa type t1451 was identified in a poultry farmer with abscesses and septic arthritis (46).…”

“…Whereas resistance toward antibiotics and heavy metals as well as the general pathogenic potential of MRSA CC398 has been thoroughly investigated (10)(11)(12)(13), the factors driving the epidemic of this clonal lineage in humans are only slightly understood. Interestingly, differences in the content of mobile genetic elements (MGEs) between the ancestral methicillin-susceptible CC398 clade that originated in humans, the methicillinresistant livestock-associated CC398 clade, and an emerging methicillin-susceptible humanspecific CC398 clade have been described previously (14)(15)(16). In the livestock-associated CC398 clade, the staphylococcal cassette chromosome mec (SCCmec) types IV and V, the of the epidemic (2000 to 2006), all available MRSA spa-CC011 isolates were included (n ϭ 92).…”

Ecological and Evolutionary Benefits of Temperate Phage: What Does or Doesn't Kill You Makes You Stronger

“…[28] Carriage of multiple prophages -polylysogeny -is common among pathogens, allowing acquisition of multiple traits and contributing to diversity in disease pathology. [29][30][31] Prophage acquisition plays an important role in the contemporary evolution of a range of pathogens. More than half of the genome variation in group A Streptococcus (GAS) strains, each of which is responsible for a characteristic array of syndromes from toxic shock syndrome and necrotizing fasciitis, Figure 1.…”

“…[30] Shifts in disease serotypes associated with acquisition of new prophages have been observed in real time in Streptococcus [32,33] and S. aureus. [29] Temperate phages frequently encode antibiotic resistance genes and lysis induced by exposure to antibiotics has been shown to lead to mobilization of antibiotic resistance genes between bacterial hosts in the animal gut. [34] It is possible that the high proportion of prophages linked to pathogen associated traits represents a bias in the literature rather than a real biological phenomenon, indeed greater sequencing of environmental samples has revealed some surprising examples of phageencoded traits, including photosynthetic genes carried by a cyanophage.…”