Overlapping Streptococcus pyogenes and Streptococcus dysgalactiae subspecies equisimilis household transmission and mobile genetic element exchange

Ouli Xie; Cameron Zachreson; Gerry Tonkin-Hill; David J Price; Jake A Lacey; Jacqueline M Morris; Malcolm I McDonald; Asha C Bowen; Philip M Giffard; Bart J Currie; Jonathan R Carapetis; Deborah C Holt; Stephen D Bentley; Mark R Davies; Steven Y C Tong

doi:10.1038/s41467-024-47816-1

Overlapping Streptococcus pyogenes and Streptococcus dysgalactiae subspecies equisimilis household transmission and mobile genetic element exchange

Nat Commun. 2024 Apr 24;15(1):3477. doi: 10.1038/s41467-024-47816-1.

Authors

Ouli Xie^{1

2}, Cameron Zachreson³, Gerry Tonkin-Hill⁴, David J Price^{1

5}, Jake A Lacey^{1

6}, Jacqueline M Morris⁶, Malcolm I McDonald⁷, Asha C Bowen⁸, Philip M Giffard^{9

10}, Bart J Currie^{9

11}, Jonathan R Carapetis⁸, Deborah C Holt⁹, Stephen D Bentley¹², Mark R Davies^#⁶, Steven Y C Tong^#^{13

14}

Affiliations

¹ Department of Infectious Diseases, University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.
² Monash Infectious Diseases, Monash Health, Melbourne, VIC, Australia.
³ School of Computing and Information Systems, University of Melbourne, Melbourne, VIC, Australia.
⁴ Department of Biostatistics, University of Oslo, Oslo, Norway.
⁵ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, VIC, Australia.
⁶ Department of Microbiology and Immunology, University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia.
⁷ Division of Tropical Health and Medicine, James Cook University, Townsville, QLD, Australia.
⁸ Wesfarmers Centre for Vaccines and Infectious Diseases, Telethon Kids Institute, University of Western Australia and Perth Children's Hospital, Perth, WA, Australia.
⁹ Global and Tropical Health Division, Menzies School of Health Research, Charles Darwin University, Darwin, NT, Australia.
¹⁰ Faculty of Health, Charles Darwin University, Darwin, NT, Australia.
¹¹ Infectious Diseases Department, Royal Darwin Hospital, Darwin, NT, Australia.
¹² Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton, UK.
¹³ Department of Infectious Diseases, University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia. steven.tong@unimelb.edu.au.
¹⁴ Victorian Infectious Diseases Service, The Royal Melbourne Hospital at the Peter Doherty Institute for Infection and Immunity, Melbourne, VIC, Australia. steven.tong@unimelb.edu.au.

^# Contributed equally.

Abstract

Streptococcus dysgalactiae subspecies equisimilis (SDSE) and Streptococcus pyogenes share skin and throat niches with extensive genomic homology and horizontal gene transfer (HGT) possibly underlying shared disease phenotypes. It is unknown if cross-species transmission interaction occurs. Here, we conduct a genomic analysis of a longitudinal household survey in remote Australian First Nations communities for patterns of cross-species transmission interaction and HGT. Collected from 4547 person-consultations, we analyse 294 SDSE and 315 S. pyogenes genomes. We find SDSE and S. pyogenes transmission intersects extensively among households and show that patterns of co-occurrence and transmission links are consistent with independent transmission without inter-species interference. We identify at least one of three near-identical cross-species mobile genetic elements (MGEs) carrying antimicrobial resistance or streptodornase virulence genes in 55 (19%) SDSE and 23 (7%) S. pyogenes isolates. These findings demonstrate co-circulation of both pathogens and HGT in communities with a high burden of streptococcal disease, supporting a need to integrate SDSE and S. pyogenes surveillance and control efforts.

Publication types

Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural

MeSH terms

Adolescent
Adult
Australia
Child
Child, Preschool
Drug Resistance, Bacterial / genetics
Family Characteristics
Female
Gene Transfer, Horizontal*
Genome, Bacterial / genetics
Humans
Interspersed Repetitive Sequences* / genetics
Longitudinal Studies
Male
Streptococcal Infections* / microbiology
Streptococcal Infections* / transmission
Streptococcus pyogenes* / classification
Streptococcus pyogenes* / genetics
Streptococcus pyogenes* / isolation & purification
Streptococcus* / genetics
Streptococcus* / isolation & purification
Young Adult

Supplementary concepts

Streptococcus dysgalactiae

Abstract

Publication types

MeSH terms

Supplementary concepts

Grants and funding