The phylogenetic landscape and nosocomial spread of the multidrug-resistant opportunist Stenotrophomonas maltophilia

Matthias I. Gröschel; Conor J. Meehan; Ivan Barilar; Margo Diricks; Aitor Gonzaga; Matthias Steglich; Oscar Conchillo-Solé; Isabell Christin Scherer; Uwe Mamat; Christian F. Luz; Katrien De Bruyne; Christian Utpatel; Daniel Yero; Isidre Gibert; Xavier Daura; Stefanie Kampmeier; Nurdyana Abdul Rahman; Michael Kresken; Tjip S. van der Werf; Ifey Alio; Wolfgang R. Streit; Kai Zhou; Thomas Schwartz; John W.A. Rossen; Maha R. Farhat; Ulrich E. Schaible; Ulrich Nübel; Jan Rupp; Joerg Steinmann; Stefan Niemann; Thomas A. Kohl

doi:10.1038/s41467-020-15123-0

The phylogenetic landscape and nosocomial spread of the multidrug-resistant opportunist Stenotrophomonas maltophilia

Matthias I. Gröschel, Conor J. Meehan, Ivan Barilar, Margo Diricks, Aitor Gonzaga, Matthias Steglich, Oscar Conchillo-Solé, Isabell Christin Scherer, Uwe Mamat, Christian F. Luz, Katrien De Bruyne, Christian Utpatel, Daniel Yero, Isidre Gibert, Xavier Daura, Stefanie Kampmeier, Nurdyana Abdul Rahman, Michael Kresken, Tjip S. van der Werf, Ifey AlioWolfgang R. Streit, Kai Zhou, Thomas Schwartz, John W.A. Rossen, Maha R. Farhat, Ulrich E. Schaible, Ulrich Nübel, Jan Rupp, Joerg Steinmann, Stefan Niemann^*, Thomas A. Kohl

^*Corresponding author for this work

Clinic of Infectious Diseases and Microbiology

101 Citations (Scopus)

Abstract

Recent studies portend a rising global spread and adaptation of human- or healthcare-associated pathogens. Here, we analyse an international collection of the emerging, multidrug-resistant, opportunistic pathogen Stenotrophomonas maltophilia from 22 countries to infer population structure and clonality at a global level. We show that the S. maltophilia complex is divided into 23 monophyletic lineages, most of which harbour strains of all degrees of human virulence. Lineage Sm6 comprises the highest rate of human-associated strains, linked to key virulence and resistance genes. Transmission analysis identifies potential outbreak events of genetically closely related strains isolated within days or weeks in the same hospitals.

Original language	English
Article number	2044
Journal	Nature Communications
Volume	11
Issue number	1
Pages (from-to)	2044
ISSN	1751-8628
DOIs	https://doi.org/10.1038/s41467-020-15123-0
Publication status	Published - 01.12.2020

Funding

We thank V. Mohr, F. Boysen and T. Ubben for technical assistance during next-generation sequencings. Parts of the work have been funded by grants from German Center for Infection Research, Federal Ministry of Education and Research, Germany, from Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy–EXC 22167-390884018, the Cluster Precision Medicine in Chronic Inflammation, and grants from the Leibniz Science Campus Evo-LUNG; I.A. and W.R.S. received funds from the University of Hamburg; C.F.L. and J.W.A.R. were funded through the European Commission Horizon 2020 Framework Marie Skłodowska-Curie Actions (Grant agreement number: 713660 - PRONKJE-WAIL - H2020-MSCA-COFUND-2015); C.J.M. was funded by the Department of Economy, Science and Innovation of the Flemish Government and the Belgian Science Policy (Belspo); K.Z. was funded by the National Natural Science Foundation of China (grant number 81702045), and 13th Five-Year National Major Science and Technology Projects of China (grant number 2018ZX10712001); O.C.S., D.Y., I.G. and X.D. were funded by the Spanish Ministry for Science, Innovation and Universities (grant reference BIO2015-66674-R); N.A.R. was funded by the SingHealth DUKE-NUS Pathology Academic Clinical Programme Clinical Innovation Support Grant (09/FY2017/P1/06-A20); U.N. was funded by the EU Horizon 2020 programme, grant agreement number 643476.

Research Areas and Centers

Academic Focus: Center for Infection and Inflammation Research (ZIEL)

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Gröschel, M. I., Meehan, C. J., Barilar, I., Diricks, M., Gonzaga, A., Steglich, M., Conchillo-Solé, O., Scherer, I. C., Mamat, U., Luz, C. F., De Bruyne, K., Utpatel, C., Yero, D., Gibert, I., Daura, X., Kampmeier, S., Rahman, N. A., Kresken, M., van der Werf, T. S., ... Kohl, T. A. (2020). The phylogenetic landscape and nosocomial spread of the multidrug-resistant opportunist Stenotrophomonas maltophilia. Nature Communications, 11(1), 2044. Article 2044. https://doi.org/10.1038/s41467-020-15123-0

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title = "The phylogenetic landscape and nosocomial spread of the multidrug-resistant opportunist Stenotrophomonas maltophilia",

abstract = "Recent studies portend a rising global spread and adaptation of human- or healthcare-associated pathogens. Here, we analyse an international collection of the emerging, multidrug-resistant, opportunistic pathogen Stenotrophomonas maltophilia from 22 countries to infer population structure and clonality at a global level. We show that the S. maltophilia complex is divided into 23 monophyletic lineages, most of which harbour strains of all degrees of human virulence. Lineage Sm6 comprises the highest rate of human-associated strains, linked to key virulence and resistance genes. Transmission analysis identifies potential outbreak events of genetically closely related strains isolated within days or weeks in the same hospitals.",

author = "Gr{\"o}schel, \{Matthias I.\} and Meehan, \{Conor J.\} and Ivan Barilar and Margo Diricks and Aitor Gonzaga and Matthias Steglich and Oscar Conchillo-Sol{\'e} and Scherer, \{Isabell Christin\} and Uwe Mamat and Luz, \{Christian F.\} and \{De Bruyne\}, Katrien and Christian Utpatel and Daniel Yero and Isidre Gibert and Xavier Daura and Stefanie Kampmeier and Rahman, \{Nurdyana Abdul\} and Michael Kresken and \{van der Werf\}, \{Tjip S.\} and Ifey Alio and Streit, \{Wolfgang R.\} and Kai Zhou and Thomas Schwartz and Rossen, \{John W.A.\} and Farhat, \{Maha R.\} and Schaible, \{Ulrich E.\} and Ulrich N{\"u}bel and Jan Rupp and Joerg Steinmann and Stefan Niemann and Kohl, \{Thomas A.\}",

note = "Funding Information: We thank V. Mohr, F. Boysen and T. Ubben for technical assistance during next-generation sequencings. Parts of the work have been funded by grants from German Center for Infection Research, Federal Ministry of Education and Research, Germany, from Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany{\textquoteright}s Excellence Strategy–EXC 22167-390884018, the Cluster Precision Medicine in Chronic Inflammation, and grants from the Leibniz Science Campus Evo-LUNG; I.A. and W.R.S. received funds from the University of Hamburg; C.F.L. and J.W.A.R. were funded through the European Commission Horizon 2020 Framework Marie Sk{\l}odowska-Curie Actions (Grant agreement number: 713660 - PRONKJE-WAIL - H2020-MSCA-COFUND-2015); C.J.M. was funded by the Department of Economy, Science and Innovation of the Flemish Government and the Belgian Science Policy (Belspo); K.Z. was funded by the National Natural Science Foundation of China (grant number 81702045), and 13th Five-Year National Major Science and Technology Projects of China (grant number 2018ZX10712001); O.C.S., D.Y., I.G. and X.D. were funded by the Spanish Ministry for Science, Innovation and Universities (grant reference BIO2015-66674-R); N.A.R. was funded by the SingHealth DUKE-NUS Pathology Academic Clinical Programme Clinical Innovation Support Grant (09/FY2017/P1/06-A20); U.N. was funded by the EU Horizon 2020 programme, grant agreement number 643476. Publisher Copyright: {\textcopyright} 2020, The Author(s). Copyright: Copyright 2020 Elsevier B.V., All rights reserved.",

year = "2020",

month = dec,

day = "1",

doi = "10.1038/s41467-020-15123-0",

language = "English",

volume = "11",

pages = "2044",

journal = "Nature Communications",

issn = "1751-8628",

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Gröschel, MI, Meehan, CJ, Barilar, I, Diricks, M, Gonzaga, A, Steglich, M, Conchillo-Solé, O, Scherer, IC, Mamat, U, Luz, CF, De Bruyne, K, Utpatel, C, Yero, D, Gibert, I, Daura, X, Kampmeier, S, Rahman, NA, Kresken, M, van der Werf, TS, Alio, I, Streit, WR, Zhou, K, Schwartz, T, Rossen, JWA, Farhat, MR, Schaible, UE, Nübel, U, Rupp, J, Steinmann, J, Niemann, S & Kohl, TA 2020, 'The phylogenetic landscape and nosocomial spread of the multidrug-resistant opportunist Stenotrophomonas maltophilia', Nature Communications, vol. 11, no. 1, 2044, pp. 2044. https://doi.org/10.1038/s41467-020-15123-0

TY - JOUR

T1 - The phylogenetic landscape and nosocomial spread of the multidrug-resistant opportunist Stenotrophomonas maltophilia

AU - Gröschel, Matthias I.

AU - Meehan, Conor J.

AU - Barilar, Ivan

AU - Diricks, Margo

AU - Gonzaga, Aitor

AU - Steglich, Matthias

AU - Conchillo-Solé, Oscar

AU - Scherer, Isabell Christin

AU - Mamat, Uwe

AU - Luz, Christian F.

AU - De Bruyne, Katrien

AU - Utpatel, Christian

AU - Yero, Daniel

AU - Gibert, Isidre

AU - Daura, Xavier

AU - Kampmeier, Stefanie

AU - Rahman, Nurdyana Abdul

AU - Kresken, Michael

AU - van der Werf, Tjip S.

AU - Alio, Ifey

AU - Streit, Wolfgang R.

AU - Zhou, Kai

AU - Schwartz, Thomas

AU - Rossen, John W.A.

AU - Farhat, Maha R.

AU - Schaible, Ulrich E.

AU - Nübel, Ulrich

AU - Rupp, Jan

AU - Steinmann, Joerg

AU - Niemann, Stefan

AU - Kohl, Thomas A.

N1 - Funding Information: We thank V. Mohr, F. Boysen and T. Ubben for technical assistance during next-generation sequencings. Parts of the work have been funded by grants from German Center for Infection Research, Federal Ministry of Education and Research, Germany, from Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy–EXC 22167-390884018, the Cluster Precision Medicine in Chronic Inflammation, and grants from the Leibniz Science Campus Evo-LUNG; I.A. and W.R.S. received funds from the University of Hamburg; C.F.L. and J.W.A.R. were funded through the European Commission Horizon 2020 Framework Marie Skłodowska-Curie Actions (Grant agreement number: 713660 - PRONKJE-WAIL - H2020-MSCA-COFUND-2015); C.J.M. was funded by the Department of Economy, Science and Innovation of the Flemish Government and the Belgian Science Policy (Belspo); K.Z. was funded by the National Natural Science Foundation of China (grant number 81702045), and 13th Five-Year National Major Science and Technology Projects of China (grant number 2018ZX10712001); O.C.S., D.Y., I.G. and X.D. were funded by the Spanish Ministry for Science, Innovation and Universities (grant reference BIO2015-66674-R); N.A.R. was funded by the SingHealth DUKE-NUS Pathology Academic Clinical Programme Clinical Innovation Support Grant (09/FY2017/P1/06-A20); U.N. was funded by the EU Horizon 2020 programme, grant agreement number 643476. Publisher Copyright: © 2020, The Author(s). Copyright: Copyright 2020 Elsevier B.V., All rights reserved.

PY - 2020/12/1

Y1 - 2020/12/1

N2 - Recent studies portend a rising global spread and adaptation of human- or healthcare-associated pathogens. Here, we analyse an international collection of the emerging, multidrug-resistant, opportunistic pathogen Stenotrophomonas maltophilia from 22 countries to infer population structure and clonality at a global level. We show that the S. maltophilia complex is divided into 23 monophyletic lineages, most of which harbour strains of all degrees of human virulence. Lineage Sm6 comprises the highest rate of human-associated strains, linked to key virulence and resistance genes. Transmission analysis identifies potential outbreak events of genetically closely related strains isolated within days or weeks in the same hospitals.

AB - Recent studies portend a rising global spread and adaptation of human- or healthcare-associated pathogens. Here, we analyse an international collection of the emerging, multidrug-resistant, opportunistic pathogen Stenotrophomonas maltophilia from 22 countries to infer population structure and clonality at a global level. We show that the S. maltophilia complex is divided into 23 monophyletic lineages, most of which harbour strains of all degrees of human virulence. Lineage Sm6 comprises the highest rate of human-associated strains, linked to key virulence and resistance genes. Transmission analysis identifies potential outbreak events of genetically closely related strains isolated within days or weeks in the same hospitals.

UR - https://www.scopus.com/pages/publications/85083972595

U2 - 10.1038/s41467-020-15123-0

DO - 10.1038/s41467-020-15123-0

M3 - Journal articles

C2 - 32341346

AN - SCOPUS:85083972595

SN - 1751-8628

VL - 11

SP - 2044

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 2044

ER -

The phylogenetic landscape and nosocomial spread of the multidrug-resistant opportunist Stenotrophomonas maltophilia

Abstract

Funding

Research Areas and Centers

UN SDGs

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