Patterns of cross-resistance and collateral sensitivity between clinical antibiotics and natural antimicrobials

Abigail Colclough; Jukka Corander; Samuel K. Sheppard; Sion C. Bayliss; Michiel Vos

doi:10.1111/eva.12762

Patterns of cross-resistance and collateral sensitivity between clinical antibiotics and natural antimicrobials

Abigail Colclough, Jukka Corander, Samuel K. Sheppard, Sion C. Bayliss, Michiel Vos^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

23 Citations (Scopus)

Abstract

Bacteria interact with a multitude of other organisms, many of which produce antimicrobials. Selection for resistance to these antimicrobials has the potential to result in resistance to clinical antibiotics when active compounds target the same bacterial pathways. The possibility of such cross-resistance between natural antimicrobials and antibiotics has to our knowledge received very little attention. The antimicrobial activity of extracts from seaweeds, known to be prolific producers of antimicrobials, is here tested against Staphylococcus aureus isolates with varied clinical antibiotic resistance profiles. An overall effect consistent with cross-resistance is demonstrated, with multidrug-resistant S. aureus strains being on average more resistant to seaweed extracts. This pattern could potentially indicate that evolution of resistance to antimicrobials in the natural environment could lead to resistance against clinical antibiotics. However, patterns of antimicrobial activity of individual seaweed extracts vary considerably and include collateral sensitivity, where increased resistance to a particular antibiotic is associated with decreased resistance to a particular seaweed extract. Our correlation-based methods allow the identification of antimicrobial extracts bearing most promise for downstream active compound identification and pharmacological testing.

Original language	English
Pages (from-to)	878-887
Number of pages	10
Journal	Evolutionary Applications
Volume	12
Issue number	5
DOIs	https://doi.org/10.1111/eva.12762
Publication status	Published - Jun 2019

Bibliographical note

Funding Information:
Microbiology Department of the Royal Cornwall Hospital in Truro for kindly providing bacterial isolates; Ruth Airs, Angus Buckling, Elze Hesse, Chris Lowe, Alan McNally and Mathias Middelboe for commenting on an earlier version of this manuscript; and David Fenwick Sr. for help with seaweed identification. AC and MV de‐ signed experiments, AC performed experiments, AC, JC, AM, SH, SB and MV analysed data, MV wrote the paper with input from AC, JC, AM, SH and SB. MV was funded by Natural Environment Research Council (NERC) grant NE/L013177/1. SS was supported by Medical Research Council (MRC) Cloud Infrastructure for Microbial Bioinformatics (grant number: MR/L015080/1). J.C. was partially funded by the COIN Centre of Excellence, Academy of Finland.

Funding Information:
We thank John Lee, Richard Bendall and colleagues at the Clinical Microbiology Department of the Royal Cornwall Hospital in Truro for kindly providing bacterial isolates; Ruth Airs, Angus Buckling, Elze Hesse, Chris Lowe, Alan McNally and Mathias Middelboe for commenting on an earlier version of this manuscript; and David Fenwick Sr. for help with seaweed identification. AC and MV designed experiments, AC performed experiments, AC, JC, AM, SH, SB and MV analysed data, MV wrote the paper with input from AC, JC, AM, SH and SB. MV was funded by Natural Environment Research Council (NERC) grant NE/L013177/1. SS was supported by Medical Research Council (MRC) Cloud Infrastructure for Microbial Bioinformatics (grant number: MR/L015080/1). J.C. was partially funded by the COIN Centre of Excellence, Academy of Finland.

Publisher Copyright:
© 2019 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd

Keywords

antibiotic resistance
Antimicrobials
collateral sensitivity
cross-resistance
seaweeds
Staphylococcus aureus

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title = "Patterns of cross-resistance and collateral sensitivity between clinical antibiotics and natural antimicrobials",

abstract = "Bacteria interact with a multitude of other organisms, many of which produce antimicrobials. Selection for resistance to these antimicrobials has the potential to result in resistance to clinical antibiotics when active compounds target the same bacterial pathways. The possibility of such cross-resistance between natural antimicrobials and antibiotics has to our knowledge received very little attention. The antimicrobial activity of extracts from seaweeds, known to be prolific producers of antimicrobials, is here tested against Staphylococcus aureus isolates with varied clinical antibiotic resistance profiles. An overall effect consistent with cross-resistance is demonstrated, with multidrug-resistant S. aureus strains being on average more resistant to seaweed extracts. This pattern could potentially indicate that evolution of resistance to antimicrobials in the natural environment could lead to resistance against clinical antibiotics. However, patterns of antimicrobial activity of individual seaweed extracts vary considerably and include collateral sensitivity, where increased resistance to a particular antibiotic is associated with decreased resistance to a particular seaweed extract. Our correlation-based methods allow the identification of antimicrobial extracts bearing most promise for downstream active compound identification and pharmacological testing.",

keywords = "antibiotic resistance, Antimicrobials, collateral sensitivity, cross-resistance, seaweeds, Staphylococcus aureus",

author = "Abigail Colclough and Jukka Corander and Sheppard, {Samuel K.} and Bayliss, {Sion C.} and Michiel Vos",

note = "Funding Information: Microbiology Department of the Royal Cornwall Hospital in Truro for kindly providing bacterial isolates; Ruth Airs, Angus Buckling, Elze Hesse, Chris Lowe, Alan McNally and Mathias Middelboe for commenting on an earlier version of this manuscript; and David Fenwick Sr. for help with seaweed identification. AC and MV de‐ signed experiments, AC performed experiments, AC, JC, AM, SH, SB and MV analysed data, MV wrote the paper with input from AC, JC, AM, SH and SB. MV was funded by Natural Environment Research Council (NERC) grant NE/L013177/1. SS was supported by Medical Research Council (MRC) Cloud Infrastructure for Microbial Bioinformatics (grant number: MR/L015080/1). J.C. was partially funded by the COIN Centre of Excellence, Academy of Finland. Funding Information: We thank John Lee, Richard Bendall and colleagues at the Clinical Microbiology Department of the Royal Cornwall Hospital in Truro for kindly providing bacterial isolates; Ruth Airs, Angus Buckling, Elze Hesse, Chris Lowe, Alan McNally and Mathias Middelboe for commenting on an earlier version of this manuscript; and David Fenwick Sr. for help with seaweed identification. AC and MV designed experiments, AC performed experiments, AC, JC, AM, SH, SB and MV analysed data, MV wrote the paper with input from AC, JC, AM, SH and SB. MV was funded by Natural Environment Research Council (NERC) grant NE/L013177/1. SS was supported by Medical Research Council (MRC) Cloud Infrastructure for Microbial Bioinformatics (grant number: MR/L015080/1). J.C. was partially funded by the COIN Centre of Excellence, Academy of Finland. Publisher Copyright: {\textcopyright} 2019 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd",

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language = "English",

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N2 - Bacteria interact with a multitude of other organisms, many of which produce antimicrobials. Selection for resistance to these antimicrobials has the potential to result in resistance to clinical antibiotics when active compounds target the same bacterial pathways. The possibility of such cross-resistance between natural antimicrobials and antibiotics has to our knowledge received very little attention. The antimicrobial activity of extracts from seaweeds, known to be prolific producers of antimicrobials, is here tested against Staphylococcus aureus isolates with varied clinical antibiotic resistance profiles. An overall effect consistent with cross-resistance is demonstrated, with multidrug-resistant S. aureus strains being on average more resistant to seaweed extracts. This pattern could potentially indicate that evolution of resistance to antimicrobials in the natural environment could lead to resistance against clinical antibiotics. However, patterns of antimicrobial activity of individual seaweed extracts vary considerably and include collateral sensitivity, where increased resistance to a particular antibiotic is associated with decreased resistance to a particular seaweed extract. Our correlation-based methods allow the identification of antimicrobial extracts bearing most promise for downstream active compound identification and pharmacological testing.

AB - Bacteria interact with a multitude of other organisms, many of which produce antimicrobials. Selection for resistance to these antimicrobials has the potential to result in resistance to clinical antibiotics when active compounds target the same bacterial pathways. The possibility of such cross-resistance between natural antimicrobials and antibiotics has to our knowledge received very little attention. The antimicrobial activity of extracts from seaweeds, known to be prolific producers of antimicrobials, is here tested against Staphylococcus aureus isolates with varied clinical antibiotic resistance profiles. An overall effect consistent with cross-resistance is demonstrated, with multidrug-resistant S. aureus strains being on average more resistant to seaweed extracts. This pattern could potentially indicate that evolution of resistance to antimicrobials in the natural environment could lead to resistance against clinical antibiotics. However, patterns of antimicrobial activity of individual seaweed extracts vary considerably and include collateral sensitivity, where increased resistance to a particular antibiotic is associated with decreased resistance to a particular seaweed extract. Our correlation-based methods allow the identification of antimicrobial extracts bearing most promise for downstream active compound identification and pharmacological testing.

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KW - collateral sensitivity

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KW - seaweeds

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ER -

Patterns of cross-resistance and collateral sensitivity between clinical antibiotics and natural antimicrobials

Abstract

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Keywords

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