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Stenotrophomonas maltophilia Belonging to Novel Sequence Types ST473 and ST474 in Wild Birds Inhabiting the Brazilian Amazonia

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Abstract

Stenotrophomonas maltophilia is an opportunistic human pathogen associated with nosocomial and community-acquired infections. We have conducted a microbiological and genomic surveillance study of broad-spectrum cephalosporin- and carbapenem-resistant Gram-negative bacteria colonizing wild birds inhabiting the Brazilian Amazonia. Strikingly, two S. maltophilia strains (SM79 and SM115) were identified in Plain-throated antwren (Isleria hauxwelli) passerines affected by Amazonian fragmentation and degradation. Noteworthy, SM79 and SM115 strains belonged to new sequence types (STs) ST474 and ST473, respectively, displaying resistance to broad-spectrum β-lactams, aminoglycosides and/or fluoroquinolones. In this regard, resistome analysis confirmed efflux pumps (smeABC, smeDEF, emrAB-tolC and macB), blaL1 and blaL2, aph(3’)-IIc and aac(6’)-Iak, and Smqnr resistance genes. Comparative phylogenomic analysis with publicly available S. maltophilia genomes clustered ST473 and ST474 with human strains, whereas the ST474 was also grouped with S. maltophilia strains isolated from water and poultry samples. In summary, we report two novel sequence types of S. maltophilia colonizing wild Amazonian birds. The presence of opportunistic multidrug-resistant pathogens in wild birds, from remotes areas, could represent an ecological problem since these animals could easily promote long-distance dispersal of medically important antimicrobial-resistant bacteria. Therefore, while our results could provide a baseline for future epidemiological genomic studies, considering the limited information regarding S. maltophilia circulating among wild animals, additional studies are necessary to evaluate the clinical impact and degree of pathogenicity of this human opportunistic pathogen in wild birds.

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Fig. 1

Data Availability

The raw sequence data and whole genome assemblies generated duringthe current study are available in the National Center for Biotechnology Information (NCBI) assembly accession numbers correspond to GCA_027941455.1 and GCA_027941475.1, respectively.

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Acknowledgements

We thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) and Conselho Nacional de Desenvolvimento Científico e Tecnológico. The authors thank Cefar Diagnóstica Ltda (São Paulo, Brazil) and CEFAP-GENIAL facility for kindly supplying antibiotic disks for susceptibility testing and Illumina sequencing, respectively. Nilton Lincopan is a research fellow of CNPq (314336/2021-4). We are grateful to Wilson Neto for the support provided during the field trips in Fazenda Fartura.

Funding

This study was supported by the Fundação de Amparo à Pesquisa do Estado de São Paulo (2020/08224-9 and 2019/15578-4), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq,422984/2021-3, and 314336/2021-4), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). Gislaine Dalazen, Fábio Parra Sellera, Herrison Fontana and Brenda Cardoso are research fellows of CAPES (88882.333521/2019-01, 88887.463868/2019-00, 88887.506496/2020-00 and 88882.333054/2019-01, respectively). Danny Fuentes-Castillo was a research fellow of Comisión Nacional de Investigación Científica y Tecnológica (CONICYT BCH 72170436). Fernanda Esposito is a research fellow of FAPESP (2019/15578-4). Nilton Lincopan is a research fellow of CNPq (314336/2021-4).

Author information

Authors and Affiliations

  1. Laboratory of Wildlife Comparative Pathology, Department of Pathology, School of Veterinary Medicine and Animal Sciences, University of São Paulo, São Paulo, Brazil

    Gislaine Dalazen & Eliana Reiko Matushima

  2. One Health Brazilian Resistance Project (OneBR), São Paulo, Brazil

    Fábio Parra Sellera, Danny Fuentes-Castillo, Elder Sano, Herrison Fontana, Brenda Cardoso, Fernanda Esposito & Nilton Lincopan

  3. Department of Internal Medicine, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil

    Fábio Parra Sellera

  4. School of Veterinary Medicine, Metropolitan University of Santos, Santos, Brazil

    Fábio Parra Sellera

  5. Departamento de Patología y Medicina Preventiva, Facultad de Ciencias Veterinarias, Universidad de Concepción, Chillán, Chile

    Danny Fuentes-Castillo

  6. Department of Clinical Analysis, Faculty of Pharmacy, University of São Paulo, São Paulo, Brazil

    Elder Sano, Herrison Fontana, Fernanda Esposito & Nilton Lincopan

  7. Department of Microbiology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil

    Brenda Cardoso & Nilton Lincopan

  8. Zoology Museum of the University of São Paulo, University of São Paulo, São Paulo, Brazil

    Luis Fábio Silveira

Authors
  1. Gislaine Dalazen
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  2. Fábio Parra Sellera
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  3. Danny Fuentes-Castillo
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  6. Brenda Cardoso
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  8. Luis Fábio Silveira
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  9. Eliana Reiko Matushima
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  10. Nilton Lincopan
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Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Gislaine Dalazen, Fábio Parra Sellera, Danny Fuentes-Castillo, Elder Sano, Herrison Fontana, Brenda Cardoso, Fernanda Esposito, Luis Fábio Silveira, Eliana Reiko Matushima, and Nilton Lincopan. The first draft of the manuscript was written by Gislaine Dalazen and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Gislaine Dalazen or Nilton Lincopan.

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Conflict of interest

The authors declare that that there is no conflict of interest.

Ethical Approval

Ethical approval was received from School of Veterinary Medicine and Animal Science of the University of São Paulo (No. 5625041119). This study was carried out in compliance with the System Authorization and Information on Biodiversity (SISBIO) of the Brazilian Institute of Environment and Renewable Natural Resources (IBAMA, License Number: 10013-5).

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Dalazen, G., Sellera, F.P., Fuentes-Castillo, D. et al. Stenotrophomonas maltophilia Belonging to Novel Sequence Types ST473 and ST474 in Wild Birds Inhabiting the Brazilian Amazonia. Curr Microbiol 81, 20 (2024). https://doi.org/10.1007/s00284-023-03532-5

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