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Insights into the role of phages on the bacterial resistome

English title Insights into the role of phages on the bacterial resistome
Applicant Gomez-Sanz Elena
Number 167090
Funding scheme NRP 72 Antimicrobial Resistance
Research institution Institut f. Umwelt und natürliche Ressourcen Zürcher Hochschule für angewandte Wissenschaften (ZHAW)
Institution of higher education ETH Zurich - ETHZ
Main discipline Molecular Biology
Start/End 01.01.2017 - 31.08.2021
Approved amount 417'307.00
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All Disciplines (2)

Discipline
Molecular Biology
Environmental Research

Keywords (7)

Antimicrobial resistance ecology; Horizontal gene transfer; Mobile genetic elements; Resistome; Metaviromics; Metagenomics; Plasmidome

Lay Summary (German)

Lead
Auch in natürlichen Ökosystemen entstehen und verbreiten sich Resistenzen. Und sie werden aus diesen in Systeme übertragen, in die der Mensch eingebunden ist. Wir klären, welche Rolle Bakterienviren, sogenannte Bakteriophagen, bei diesen Prozessen spielen.
Lay summary

Für die Zunahme von Antibiotikaresistenzen wird oft ausschliesslich der Einsatz von antimikrobiellen Substanzen durch den Menschen verantwortlich gemacht. Doch auch in unberührten Böden und Gewässern finden sich Gene, die Bakterien gegenüber Antibiotika resistent machen. Es ist anzunehmen, dass der Ursprung für einige Resistenzen in der Humanmedizin in diesen Ökosystemen liegt. Wir untersuchen, wie viel und welche Resistenzen in Böden und Gewässern vorkommen, und wie sie zwischen Mikroorganismen übertragen werden. Dabei fokussieren wir auf Bakterienviren, sogenannte Bakteriophagen. Diese spielen eine wichtige Rolle beim Austausch von genetischem Material zwischen Bakterien und könnten auch für den Transfer von Resistenzgenen zwischen verschiedenen Ökosystemen verantwortlich sein.

Hintergrund
Bisher wurden antimikrobielle Resistenzen, die in natürlichen Ökosystemen vorkommen, kaum in Zusammenhang mit der aktuellen Resistenzproblematik gebracht. Doch neuere Studien weisen darauf hin, dass wichtige Verbindungen existieren. Vor allem Bakteriophagen könnten dabei von grosser Bedeutung zu sein.

Ziel
Wir wollen klären, welche Rolle Bakteriophagen bei der Verbreitung von Antibiotikaresistenzen in und zwischen natürlichen Ökosystemen spielen, und wie wichtig sie dabei im Verhältnis zu anderen Verbreitungsmechanismen sind. Ein weiteres Ziel ist, Tests zu entwickeln, die von Bakteriophagen übertragene Resistenzgene erkennen.

Bedeutung
Ein detailliertes Verständnis darüber, wie bakterielle Resistenzen sich in und zwischen verschiedenen – auch natürlichen – Ökosystemen entwickeln und verbreiten, kann entscheidende Hinweise liefern, um solche Prozesse zu verhindern.

Direct link to Lay Summary Last update: 08.12.2017

Lay Summary (French)

Lead
Les résistances se développent et se propagent également au sein des écosystèmes naturels. A partir de ceux-ci, elles se transfèrent à des systèmes auxquels l’homme est intégré. Nous étudions le rôle que les virus bactériens - ou bactériophages - jouent dans ces processus.
Lay summary

L’augmentation des résistances aux antibiotiques est souvent exclusivement imputée à l’utilisation médicale de substances antimicrobiennes. Dans les sols et les eaux préservés, il existe néanmoins des gènes qui rendent les bactéries résistantes aux antimicrobiens. Il est probable que ces écosystèmes sont à l’origine de certaines des résistances observées en médecine humaine. Nous étudions quelles sont celles qui prévalent et en quelle quantité dans les sols et les eaux, et analysons les modes de transmission entre micro-organismes. Nous nous focalisons ce faisant sur les virus bactériens (bactériophages). Ceux-ci jouent un rôle essentiel dans les échanges de matériel génétique entre bactéries et pourraient être responsables du transfert de gènes de résistance entre les écosystèmes.

Contexte
Jusqu’à présent, une relation n’a que rarement été établie entre les résistances antimicrobiennes observées dans les écosystèmes naturels et la problématique de résistance actuellement rencontrée. Des études récentes indiquent cependant qu’il existe des liens étroits entre ces deux phénomènes et que les bactériophages pourraient y jouer un rôle significatif.

Objectif
Nous souhaitons établir quel rôle les bactériophages jouent dans la propagation des résistances aux antibiotiques dans et entre les écosystèmes naturels et déterminer leur prépondérance par rapport à d’autres mécanismes de propagation. Nous visons également à développer des tests permettant de reconnaître les gènes de résistance transmis par les virus bactériens.

Importance
Une compréhension détaillée de la manière dont les résistances se développent et se propagent dans et entre les différents écosystèmes – qu’ils soient ou non naturels – peut fournir des indications décisives pour prévenir ces phénomènes.

Direct link to Lay Summary Last update: 08.12.2017

Lay Summary (English)

Lead
Some resistance determinants to antibiotics seem to develop and spread in natural eco-systems, which are later transferred to human related systems. We clarify the role that bacterial viruses, so-called bacteriophages, play in these processes.
Lay summary

The use of antimicrobials by humans is often named as the sole reason for the emergence and rise of antimicrobial resistance. However, genes that make bacteria resistant to antibiotics can also be found in virgin soils and bodies of water. It can be assumed that the origin of some of the resistances encountered in human medicine lies in these eco-systems. We investigate the resistance load in soils and bodies of water and how resistance is transferred between micro-organisms living in them. Our main focus is on bacterial viruses, so-called bacteriophages. They play an important role in the exchange of genetic material between bacteria, and they could also be responsible for the transfer of resistance genes between different eco-systems.

Background
To date, antimicrobial resistance found in natural eco-systems has hardly been associated with current resistance problems. Recent studies, however, indicate the possible existence of important connections, for which bacteriophages might be of particular significance. 

Aim
We want to clarify the role played by bacteriophages in the spread of antibacterial resistance in and between different eco-systems and its relative burden with regards to other transfer mechanisms. A further objective is the development of tests that detect and characterise such bacteriophage located resistance genes.

Relevance
A detailed understanding of how bacterial resistance emerge in and between different eco-systems – including natural systems – can provide decisive indicators on how to prevent these processes.

Direct link to Lay Summary Last update: 08.12.2017

Responsible applicant and co-applicants

Employees

Project partner

Publications

Publication
The Resistome and Mobilome of Multidrug-Resistant Staphylococcus sciuri C2865 Unveil a Transferable Trimethoprim Resistance Gene, Designated dfrE, Spread Unnoticed
Gómez SanzElena, Haro-MorenoJose Manuel, JensenSlade O., Roda-GarciaJuan J., Lopez-PerezMario (2021), The Resistome and Mobilome of Multidrug-Resistant Staphylococcus sciuri C2865 Unveil a Transferable Trimethoprim Resistance Gene, Designated dfrE, Spread Unnoticed, in mSystems, 6(4), e00511-21.
Natural phage communities crosslink different species within the genus Staphylococcus
Göller1 Pauline C, Elsener Tabea, Lorgé Dominic, Radulovic Natasa, Bernardi Viona, Naumann Annika, Amri Nesrine, Khatchatourova Ekaterina, Hernandes Coutinho Felipe, Loessner Martin J, Gómez Sanz Elena (2021), Natural phage communities crosslink different species within the genus Staphylococcus, 1.
Uncovering a hidden diversity: optimized protocols for the extraction of dsDNA bacteriophages from soil
Göller Pauline C., Haro-Moreno Jose M., Rodriguez-Valera Francisco, Loessner Martin J., Gómez-Sanz Elena (2020), Uncovering a hidden diversity: optimized protocols for the extraction of dsDNA bacteriophages from soil, in Microbiome, 8(1), 17-17.
Staphylococcus sciuri C2865 from a distinct subspecies cluster as reservoir of the novel transferable trimethoprim resistance gene, dfrE, and adaptation driving mobile elements
Gómez-Sanz Elena, Haro-Moreno Jose Manuel, Jensen Slade O, Roda-Garcia Juan Jose, Lopez-Perez Mario (2020), Staphylococcus sciuri C2865 from a distinct subspecies cluster as reservoir of the novel transferable trimethoprim resistance gene, dfrE, and adaptation driving mobile elements, 1.
Uncovering a hidden diversity: optimized protocols for the extraction of dsDNA bacteriophages from soil
Göller Pauline C, Haro-Moreno Jose M, Rodriguez-Valera Francisco, Loessner Martin J, Gómez-Sanz Elena (2019), Uncovering a hidden diversity: optimized protocols for the extraction of dsDNA bacteriophages from soil, in BioRxiv, 1.
Multi-species host range of staphylococcal phages isolated from wastewater
GöllerPauline C, ElsenerTabea, LorgéDominic, RadulovicNatasa, BernardiViona, NaumannAnnika, AmriNesrine, KhatchatourovaEkaterina, Hernandes CoutinhoFelipe, LoessnerMartin J, Gómez SanzElena, Multi-species host range of staphylococcal phages isolated from wastewater, in Nature Communications, 1.

Collaboration

Group / person Country
Types of collaboration
Prof. Carmen Torres / Department of Agriculture and Food / University of La Rioja / Logroño Spain (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
Dr. Jochen Mayer / Nutrient Flows / Institute for Sustainability Sciences, Agroscope, Zürich Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
- Research Infrastructure
A/Prof. Slade O. Jensen / Department of Microbiology & Infectious Diseases / Ingham Institute Locked Australia (Oceania)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Maite Muniesa / Department of Microbiology / University of Barcelona / Barcelona Spain (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Dr. Diana Gutierrez / Instituto de Productos Lácteos de Asturias (IPLA-CSIC), Villaviciosa, Asturias Spain (Europe)
- in-depth/constructive exchanges on approaches, methods or results
Prof. Vincent Perreten / Institute of Veterinary Bacteriology Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results
- Publication
Dr. Antonella Demarta / SUPSI-Laboratory of Applied Microbiology Switzerland (Europe)
- in-depth/constructive exchanges on approaches, methods or results

Scientific events

Active participation

Title Type of contribution Title of article or contribution Date Place Persons involved
Swiss Society for Microbiology - Annual Meeting and Assembly 2021 Poster Natural phage communities crosslink different species within the genus Staphylococcus 02.09.2021 virtual, Switzerland Göller Pauline Carlotta; Gomez-Sanz Elena;
EAWAG Surf seminar series (ETH domain) Individual talk Insights into the Role of Phages on the Bacterial Resistome 16.12.2019 Kastanienbaum, Switzerland Gomez-Sanz Elena;
University Hospital Ramon y Cajal seminar series Individual talk Bacteriófagos: arma de doble filo en la lucha contra la resistencia a los antibióticos 02.12.2019 Madrid, Spain Gomez-Sanz Elena;
Invited Seminar for Doctoral Program in Biomedical and Biotechnological Sciences - New Challenges Biotechnology Health Individual talk BACTERIÓFAGOS: arma de doble filo en la lucha contra la resistencia a los antibióticos 28.11.2019 Logrono, Spain Gomez-Sanz Elena;
III Jornada Uso Prudente de los Antibioticos y Resistencia Bacteriana Individual talk DESARROLLO DE ALTERNATIVAS AL USO DE ANTIBIÓTICOS CONVENCIONALES: Bacteriófagos y sus derivados 18.11.2019 Logrono, Spain Gomez-Sanz Elena;
Institute of Food, Nutrition and Health (IFNH) seminar series (ETHZ) Individual talk Tackling Antimicrobial Resistance from the One Health Approach 12.11.2019 Zurich, Switzerland Gomez-Sanz Elena;
Swiss Society for Microbiology - Annual Meeting and Assembly 2019 Poster Uncovering a hidden diversity: optimization protocols for the extraction of bacteriophages from soil 03.09.2019 Zurich, Switzerland Göller Pauline Carlotta; Loessner Martin; Gomez-Sanz Elena;
MSCA IF Cluster Event on Antimicrobial Resistance Talk given at a conference Insights into the Role of Phages on the Bacterial Resistome 26.06.2019 Barcelona, Spain Gomez-Sanz Elena;
5th International Symposium on the Environmental Dimension of Antibiotic Resistance (EDAR5) Poster Bacterial and viral composition and antimicrobial resistance determinants in one of the oldest experimental agricultural field soils in Europe 09.06.2019 Hong Kong, China Gomez-Sanz Elena; Göller Pauline Carlotta; Loessner Martin;
Swiss Society for Microbiology - Annual Meeting and Assembly 2018 Talk given at a conference Do Long-term Land-use practices Affect Soil Bacterial and Viral Profiling, Antimicrobial Resistance Evolution and Spread? 28.08.2018 Laussane, Switzerland Loessner Martin; Gomez-Sanz Elena;
Ecology of Soil Microorganisms Poster Microbial composition and antimicrobial resistance determinants in one of the oldest experimental agricultural field soils in Europe 17.06.2018 Helsinki, Finland Loessner Martin; Gomez-Sanz Elena;
PCS 3rd Annual Health Care Conference 2018 Talk given at a conference Impact of different farming systems on the bacterial composition and on the antimicrobial and metal resistance determinants 28.04.2018 Prague, Czech Republic Gomez-Sanz Elena;
Group seminar invitation at Evolutionary Genomics Group (EGG) at the Miguel Hernandez University, San Juan de Alicante, Spain Individual talk Insights into the role of phages on the bacterial resistome 06.04.2018 San Juan de Alicante, Spain Gomez-Sanz Elena;
Seminar series for Chemistry and Biotechnology Master for the subject Pathology and Molecular Diagnostic Individual talk Antimicrobial Resistance from the One Health Perspective: Does Long-term Land-use Affect Soil Bacterial Profiling, Antimicrobial Resistance Evolution and Spread? 28.03.2018 Logroño, Spain Gomez-Sanz Elena;
Seminar in Biosciences - Training Program in Biomedicine and Technologies for Life -University of Alicante Individual talk ANTIMICROBIAL RESISTANCE FROM THE ONE HEALTH PERSPECTIVE: DOES LONG-TERM LAND-USE AFFECT SOIL BACTERIAL PROFILING, ANTIMICROBIAL RESISTANCE EVOLUTION AND SPREAD? 26.03.2018 Alicante, Spain Gomez-Sanz Elena;
20th International Conference on Pharmaceutical Biotechnology Talk given at a conference Mobilome and Resistome Analysis of Canine Multidrug Resistant Methicillin-resistant Staphylococcus sciuri Strain C2865 and Comparative Genomics of S. sciuri Species Group 07.12.2017 Madrid, Spain Gomez-Sanz Elena;
2nd ASM Conference on Rapid Applied Microbial Next-Generation Sequencing and Bioinformatic Pipelines Poster Mobilome and Resistome Analysis of Canine Multidrug Resistant Methicillin-resistant Staphylococcus sciuri Strain C2865 and Comparative Genomics of S. sciuri Species Group 08.10.2017 Washington DC, United States of America Gomez-Sanz Elena;
Joint annual meeting 2017 -Swiss Society for Microbiology SSM Talk given at a conference Mobilome and Resistome Analysis of Canine Multidrug Resistant Methicillin-resistant Staphylococcus sciuri Strain C2865 and Comparative Genomics of S. sciuri Species Group 30.08.2017 Basel, Switzerland Gomez-Sanz Elena; Loessner Martin;
4th International Symposium on the Environmental Dimension of Antibiotic Resistance Poster IMPACT OF DIFFERENT FARMING SYSTEMS ON THE ABUNDANCE AND DIVERSITY OF ANTIMICROBIAL RESISTANCE DETERMINANTS AND BACTERIAL COMMUNITY 13.08.2017 Lansing, Michigan, United States of America Gomez-Sanz Elena;
Group seminar invitation at Evolutionary Genomics Group (EGG) at the Miguel Hernandez University, San Juan de Alicante, Spain Individual talk Insights into the role of phages on the bacterial resistome 02.08.2017 San Juan de Alicante, Spain Gomez-Sanz Elena;


Knowledge transfer events

Active participation

Title Type of contribution Date Place Persons involved
Master Program in Chemistry and Biotechnology; Subject: “Pathology and Molecular Diagnosis”. University of La Rioja Performances, exhibitions (e.g. for education institutions) 19.05.2021 online, Spain Gomez-Sanz Elena;
Master Program in Biomedicine and Technologies for Life; Activity: “Research Seminars and Workshops”. Department of Microbiology, University of Alicante Performances, exhibitions (e.g. for education institutions) 31.03.2021 online, Spain Gomez-Sanz Elena;
International Day of Women and Girls in Science Poster 11.02.2021 virtual, Switzerland Gomez-Sanz Elena;
Master Program in Chemistry and Biotechnology; Subject: “New challenges in biotechnology and Health”. University of La Rioja Performances, exhibitions (e.g. for education institutions) 13.01.2021 online, Spain Gomez-Sanz Elena;
Master Program in Chemistry and Biotechnology; Subject: “Pathology and Molecular Diagnosis”. University of La Rioja Performances, exhibitions (e.g. for education institutions) 05.05.2020 online, Spain Gomez-Sanz Elena;
Bacteriophage Networking Meeting Performances, exhibitions (e.g. for education institutions) 14.12.2019 Zurich, Switzerland Loessner Martin; Gomez-Sanz Elena;
Invited Seminar for Doctoral Program in Biomedical and Biotechnological Sciences - New Challenges Biotechnology Health Talk 28.11.2019 Logrono, Spain Gomez-Sanz Elena;
III Jornada Uso Prudente de los Antibioticos y Resistencia Bacteriana Talk 18.11.2019 Logrono, Spain Gomez-Sanz Elena;
MicroTalks Constest - ACECH (Association of Spanish Scientists in Switzerland) Performances, exhibitions (e.g. for education institutions) 20.10.2018 Neuchatel, Switzerland Gomez-Sanz Elena;
Seminar series for Chemistry and Biotechnology Master for the subject Pathology and Molecular Diagnostic Performances, exhibitions (e.g. for education institutions) 28.03.2018 Logroño, Spain Gomez-Sanz Elena;
Seminar in Biosciences - Training Program in Biomedicine and Technologies for Life, University of Alicante Performances, exhibitions (e.g. for education institutions) 26.03.2018 Alicante, Spain Gomez-Sanz Elena;


Communication with the public

Communication Title Media Place Year
Media relations: print media, online media Short News "Reservoir for resistance" SNSF journal Horizons International German-speaking Switzerland 2021
New media (web, blogs, podcasts, news feeds etc.) "Behind the Paper" about Nature Communication paper 2021 Nature Research Microbiology Community International 2021
Media relations: radio, television Punto de Enlace” from Radio Exterior de España Radio Nacional de España International 2021
New media (web, blogs, podcasts, news feeds etc.) Women in Science - Yesterday and Today Association of Spanish Scientist in Switzerland (ACECH) International 2021
New media (web, blogs, podcasts, news feeds etc.) "Behind the Paper" about Microbiome paper 2020 Nature Research Microbiology Community International 2020
New media (web, blogs, podcasts, news feeds etc.) "Results in Brief" about MSCA-IF-GF ROPHARE project European Commission CORDIS website International 2020
Talks/events/exhibitions III Jornada Uso Prudente de los Antibioticos y Resistencia Bacteriana International 2019
Media relations: radio, television Investigadores por el mundo (Researchers around the world) Libertad Radio International 2019
Media relations: print media, online media La ciencia en Suiza habla español SWI-swissinfo.ch German-speaking Switzerland International 2019
Print (books, brochures, leaflets) Ciencia en el Parlamento (Science in the Parliment) - Spain International 2018
Talks/events/exhibitions MicroTalks Constest ACECH (Association of Spanish Scientists in Switzerland) Western Switzerland 2018
Media relations: radio, television "Good news of the day" Onda Cero La Rioja (Spain) International 2017
Media relations: print media, online media "La doctora Elena Gómez logra una acción Marie S. Curie" website of the University of La Rioja, Spain (university where the PI did her PhD) International 2017
Media relations: print media, online media "La investigadora del CIBIR Elena Gómez obtiene una beca Marie Curie" Regional newspaper La Rioja International 2017

Abstract

There is an imperative need to gain knowledge on the spread and evolution of antimicrobial resistance (AMR). Recent evidence from environmental, animal and human microbial studies shows that AMR is ancient and envi-ronments without contact with anthropogenic antibiotics possess abundant AMR genes. Bacteriophages are the most abundant entities in Earth and recent studies provide indirect evidence for the major role of transduction in the dissemination of AMR genes. Hence, phages might be of critical importance for evading one of the bottle-necks (ecological connectivity) that modulates the transmission of AMR genes from natural environments to animal and human biomes. In this proposal, a holistic and multidisciplinary approach that combines molecular genetics, genomics, metagenomics (and other -omics approaches), in-vitro experimental analysis, computational biology, bioinformatics analysis, and statistics will be conducted to measure the potential of phages as vehicles for antimicrobial resistance (AMR) transmission and spread in environmental systems with different antibiotic selective pressure. This comprehensive approach will allow us to better understand the phage-bacteria interac-tions that may drive AMR spread in different ecosystems. From this understanding we expect to be able to design and develop new tools and contingency actions for the control of AMR in clinical and veterinary practice as well as in agriculture.
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