Identification of source and sink populations for the emergence and global spread of the East-Asia clone of community-associated MRSA

Ward, Melissa J.; Goncheva, Mariya I.; Richardson, Emily J.; McAdam, Paul R.; Raftis, Emma J.; Kearns, Angela; Daum, Robert S.; David, Michael Z.; Lauderdale, Tsai Ling; Edwards, Giles; Nimmo, Graeme R.; Coombs, Geoffrey W.; Huijsdens, Xander W.; Woolhouse, Mark; Fitzgerald, J. Ross

doi:10.1186/s13059-016-1022-0

Cited by 39 publications

(57 citation statements)

References 72 publications

(83 reference statements)

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“…While correlation analyses act as gateways for identifying interactive relationships between microbial members, it provides no information on the environmental and strain physiological states necessary for such interactions to occur. Coupled with the recent identification of separate evolutionary patterns between continental strains of S. aureus [ 45 ], the results here again beckon the need for shotgun metagenomics sequencing to examine microbial associations at higher resolution, not only to understand species- and strain-level patterns in microbial associative relationships but also the metabolic and physiological bases for such relationships [ 10 ].…”

Section: Resultsmentioning

confidence: 81%

Individual and household attributes influence the dynamics of the personal skin microbiota and its association network

et al. 2018

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BackgroundNumerous studies have thus far characterized the temporal dynamics of the skin microbiota of healthy individuals. However, there is no information regarding the dynamics of different microbial association network properties. Also, there is little understanding of how living conditions, specifically cohabitation and household occupancy, may be associated with the nature and extent (or degree) of cutaneous microbiota change within individuals over time. In this study, the dynamics of the skin microbiota, and its association networks, on the skin of urban residents over four seasons were characterized.ResultsSimilar to western cohorts, the individuals of this cohort show different extents of variations in relative abundance of common skin colonizers, concomitant with individual- and household-associated changes in differential abundances of bacterial taxa. Interestingly, the individualized nature of the skin microbiota extends to various aspects of microbial association networks, including co-occurring and excluding taxa, as well as overall network structural properties. Household occupancy is correlated with the extent of variations in relative abundance of Propionibacterium, Acinetobacter, and Bacillus over multiple skin sites. In addition, household occupancy is also associated with the extent of temporal changes in microbial diversity and composition within a resident’s skin.ConclusionsThis is the first study investigating the potential roles household occupancy has on the extent of change in one’s cutaneous microbiota and its association network structures. In particular, we show that relationships between the skin microbiota of a resident, his/her cohabitants, and those of non-cohabitants over time are highly personal and are possibly governed by living conditions and nature of interactions between cohabitants within households over 1 year. This study calls for increased awareness to personal and lifestyle factors that may govern relationships between the skin microbiota of one individual and those of cohabitants, and changes in the microbial association network structures within a person over time. The current study will act as a baseline for future assessments in comparing against temporal dynamics of microbiota from individuals with different skin conditions and for identifying residential factors that are beneficial in promoting the dynamics of the skin microbiota associated with health.Electronic supplementary materialThe online version of this article (10.1186/s40168-018-0412-9) contains supplementary material, which is available to authorized users.

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Section: Resultsmentioning

confidence: 81%

Individual and household attributes influence the dynamics of the personal skin microbiota and its association network

et al. 2018

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“…While several MGEs have been identified to be associated with host-specific clones 18,19,22,24 Our findings suggest that since human-driven domestication, interactions with livestock have provided opportunities for numerous successful host-switch events between humans and livestock hosts. Further, industrialization of agriculture including use of antibiotics and feed supplements in intensive farming have directly influenced the evolution of S. aureus clones resulting in the emergence of resistance in response to distinct antibiotic selective pressures in human medicine and agriculture 18,38 . These data support the idea that surveillance could play a critical role in the early identification of emerging clones that have jumped host.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2018

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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.

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“…Similarly, ST80-MRSA in Europe, which likely arose from a methicillin-susceptible S. aureus (MSSA) ancestor from sub-Saharan Africa ( Stegger et al, 2014 ), has not become established in the United States. Frequent intercontinental transfers have also been noted for the South-East Asian CA-MRSA clone (ST59), but with limited evidence of ongoing clonal transmission outside the country of origin ( Ward et al, 2016 ).…”

Section: Introductionmentioning

confidence: 99%

Global Scale Dissemination of ST93: A Divergent Staphylococcus aureus Epidemic Lineage That Has Recently Emerged From Remote Northern Australia

et al. 2018

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Background: In Australia, community-associated methicillin-resistant Staphylococcus aureus (MRSA) lineage sequence type (ST) 93 has rapidly risen to dominance since being described in the early 1990s. We examined 459 ST93 genome sequences from Australia, New Zealand, Samoa, and Europe to investigate the evolutionary history of ST93, its emergence in Australia and subsequent spread overseas.Results: Comparisons with other S. aureus genomes indicate that ST93 is an early diverging and recombinant lineage, comprising of segments from the ST59/ST121 lineage and from a divergent but currently unsampled Staphylococcal population. However, within extant ST93 strains limited genetic diversity was apparent with the most recent common ancestor dated to 1977 (95% highest posterior density 1973–1981). An epidemic ST93 population arose from a methicillin-susceptible progenitor in remote Northern Australia, which has a proportionally large Indigenous population, with documented overcrowded housing and a high burden of skin infection. Methicillin-resistance was acquired three times in these regions, with a clade harboring a staphylococcal cassette chromosome mec (SCCmec) IVa expanding and spreading to Australia’s east coast by 2000. We observed sporadic and non-sustained introductions of ST93-MRSA-IVa to the United Kingdom. In contrast, in New Zealand, ST93-MRSA-IVa was sustainably transmitted with clonal expansion within the Pacific Islander population, who experience similar disadvantages as Australian Indigenous populations.Conclusion: ST93 has a highly recombinant genome including portions derived from an early diverging S. aureus population. Our findings highlight the need to understand host population factors in the emergence and spread of antimicrobial resistant community pathogens.

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Identification of source and sink populations for the emergence and global spread of the East-Asia clone of community-associated MRSA

Cited by 39 publications

References 72 publications

Individual and household attributes influence the dynamics of the personal skin microbiota and its association network

Individual and household attributes influence the dynamics of the personal skin microbiota and its association network

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

Global Scale Dissemination of ST93: A Divergent Staphylococcus aureus Epidemic Lineage That Has Recently Emerged From Remote Northern Australia

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