Detection of antimicrobial producing Staphylococcus from migratory birds: Potential role in nasotracheal microbiota modulation

A collection of 259 staphylococci of 13 different species [212 coagulase-negative (CoNS) and 47 coagulase-positive (CoPS)] recovered from nasotracheal samples of 87 healthy nestling white storks was tested by the spot-on-lawn method for antimicrobial-activity (AA) against 14 indicator bacteria. More...

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Main Authors: Rosa Fernández-Fernández, Idris Nasir Abdullahi, Carmen González-Azcona, Adriana Ulloa, Agustí Martínez, Sara García-Vela, Ursula Höfle, Myriam Zarazaga, Carmen Lozano, Carmen Torres
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-04-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1144975/full
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author Rosa Fernández-Fernández
Idris Nasir Abdullahi
Carmen González-Azcona
Adriana Ulloa
Agustí Martínez
Sara García-Vela
Sara García-Vela
Ursula Höfle
Myriam Zarazaga
Carmen Lozano
Carmen Torres
author_facet Rosa Fernández-Fernández
Idris Nasir Abdullahi
Carmen González-Azcona
Adriana Ulloa
Agustí Martínez
Sara García-Vela
Sara García-Vela
Ursula Höfle
Myriam Zarazaga
Carmen Lozano
Carmen Torres
author_sort Rosa Fernández-Fernández
collection DOAJ
description A collection of 259 staphylococci of 13 different species [212 coagulase-negative (CoNS) and 47 coagulase-positive (CoPS)] recovered from nasotracheal samples of 87 healthy nestling white storks was tested by the spot-on-lawn method for antimicrobial-activity (AA) against 14 indicator bacteria. Moreover, extracts of AP isolates were obtained [cell-free-supernatants (CFS) both crude and concentrated and butanol extracts] and tested against the 14 indicator bacteria. The microbiota modulation capacity of AP isolates was tested considering: (a) intra-sample AA, against all Gram-positive bacteria recovered in the same stork nasotracheal sample; (b) inter-sample AA against a selection of representative Gram-positive bacteria of the nasotracheal microbiota of all the storks (30 isolates of 29 different species and nine genera). In addition, enzymatic susceptibility test was carried out in selected AP isolates and bacteriocin encoding genes was studied by PCR/sequencing. In this respect, nine isolates (3.5%; seven CoNS and two CoPS) showed AA against at least one indicator bacteria and were considered antimicrobial-producing (AP) isolates. The AP isolates showed AA only for Gram-positive bacteria. Three of these AP isolates (S. hominis X3764, S. sciuri X4000, and S. chromogenes X4620) revealed AA on all extract conditions; other four AP isolates only showed activity in extracts after concentration; the remaining two AP isolates did not show AA in any of extract conditions. As for the microbiota modulation evaluation, three of the nine AP-isolates revealed intra-sample AA. It is to highlight the potent inter-sample AA of the X3764 isolate inhibiting 73% of the 29 representative Gram-positive species of the nasotracheal stork microbiota population. On the other hand, enzymatic analysis carried out in the two highest AP isolates (X3764 and X4000) verified the proteinaceous nature of the antimicrobial compound and PCR analysis revealed the presence of lantibiotic-like encoding genes in the nine AP isolates. In conclusion, these results show that nasotracheal staphylococci of healthy storks, and especially CoNS, produce antimicrobial substances that could be important in the modulations of their nasal microbiota.
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spelling doaj.art-c879bc70e170409b9d2ebd3d1473cbcc2023-04-11T04:54:13ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-04-011410.3389/fmicb.2023.11449751144975Detection of antimicrobial producing Staphylococcus from migratory birds: Potential role in nasotracheal microbiota modulationRosa Fernández-Fernández0Idris Nasir Abdullahi1Carmen González-Azcona2Adriana Ulloa3Agustí Martínez4Sara García-Vela5Sara García-Vela6Ursula Höfle7Myriam Zarazaga8Carmen Lozano9Carmen Torres10Area of Biochemistry and Molecular Biology, One Health-UR Research Group, University of La Rioja, Logroño, SpainArea of Biochemistry and Molecular Biology, One Health-UR Research Group, University of La Rioja, Logroño, SpainArea of Biochemistry and Molecular Biology, One Health-UR Research Group, University of La Rioja, Logroño, SpainArea of Biochemistry and Molecular Biology, One Health-UR Research Group, University of La Rioja, Logroño, SpainArea of Biochemistry and Molecular Biology, One Health-UR Research Group, University of La Rioja, Logroño, SpainArea of Biochemistry and Molecular Biology, One Health-UR Research Group, University of La Rioja, Logroño, SpainDepartment of Food Science, University of Laval, Québec City, QC, CanadaSaBio (Health and Biotechnology) Research Group, Game and Wildlife Research Institute, Spanish National Research Council/University of Castilla–La Mancha, Ciudad Real, SpainArea of Biochemistry and Molecular Biology, One Health-UR Research Group, University of La Rioja, Logroño, SpainArea of Biochemistry and Molecular Biology, One Health-UR Research Group, University of La Rioja, Logroño, SpainArea of Biochemistry and Molecular Biology, One Health-UR Research Group, University of La Rioja, Logroño, SpainA collection of 259 staphylococci of 13 different species [212 coagulase-negative (CoNS) and 47 coagulase-positive (CoPS)] recovered from nasotracheal samples of 87 healthy nestling white storks was tested by the spot-on-lawn method for antimicrobial-activity (AA) against 14 indicator bacteria. Moreover, extracts of AP isolates were obtained [cell-free-supernatants (CFS) both crude and concentrated and butanol extracts] and tested against the 14 indicator bacteria. The microbiota modulation capacity of AP isolates was tested considering: (a) intra-sample AA, against all Gram-positive bacteria recovered in the same stork nasotracheal sample; (b) inter-sample AA against a selection of representative Gram-positive bacteria of the nasotracheal microbiota of all the storks (30 isolates of 29 different species and nine genera). In addition, enzymatic susceptibility test was carried out in selected AP isolates and bacteriocin encoding genes was studied by PCR/sequencing. In this respect, nine isolates (3.5%; seven CoNS and two CoPS) showed AA against at least one indicator bacteria and were considered antimicrobial-producing (AP) isolates. The AP isolates showed AA only for Gram-positive bacteria. Three of these AP isolates (S. hominis X3764, S. sciuri X4000, and S. chromogenes X4620) revealed AA on all extract conditions; other four AP isolates only showed activity in extracts after concentration; the remaining two AP isolates did not show AA in any of extract conditions. As for the microbiota modulation evaluation, three of the nine AP-isolates revealed intra-sample AA. It is to highlight the potent inter-sample AA of the X3764 isolate inhibiting 73% of the 29 representative Gram-positive species of the nasotracheal stork microbiota population. On the other hand, enzymatic analysis carried out in the two highest AP isolates (X3764 and X4000) verified the proteinaceous nature of the antimicrobial compound and PCR analysis revealed the presence of lantibiotic-like encoding genes in the nine AP isolates. In conclusion, these results show that nasotracheal staphylococci of healthy storks, and especially CoNS, produce antimicrobial substances that could be important in the modulations of their nasal microbiota.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1144975/fullstaphylococcicoagulase-negative staphylococcibacteriocinsantimicrobial activitiesstorksnasal microbiota
spellingShingle Rosa Fernández-Fernández
Idris Nasir Abdullahi
Carmen González-Azcona
Adriana Ulloa
Agustí Martínez
Sara García-Vela
Sara García-Vela
Ursula Höfle
Myriam Zarazaga
Carmen Lozano
Carmen Torres
Detection of antimicrobial producing Staphylococcus from migratory birds: Potential role in nasotracheal microbiota modulation
Frontiers in Microbiology
staphylococci
coagulase-negative staphylococci
bacteriocins
antimicrobial activities
storks
nasal microbiota
title Detection of antimicrobial producing Staphylococcus from migratory birds: Potential role in nasotracheal microbiota modulation
title_full Detection of antimicrobial producing Staphylococcus from migratory birds: Potential role in nasotracheal microbiota modulation
title_fullStr Detection of antimicrobial producing Staphylococcus from migratory birds: Potential role in nasotracheal microbiota modulation
title_full_unstemmed Detection of antimicrobial producing Staphylococcus from migratory birds: Potential role in nasotracheal microbiota modulation
title_short Detection of antimicrobial producing Staphylococcus from migratory birds: Potential role in nasotracheal microbiota modulation
title_sort detection of antimicrobial producing staphylococcus from migratory birds potential role in nasotracheal microbiota modulation
topic staphylococci
coagulase-negative staphylococci
bacteriocins
antimicrobial activities
storks
nasal microbiota
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1144975/full
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