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International Journal of Molecular Sciences, volume 23, issue 3, pages 1168

Deep Functional Profiling of Wild Animal Microbiomes Reveals Probiotic Bacillus pumilus Strains with a Common Biosynthetic Fingerprint

Baranova Margarita N 1
Mokrushina Yuliana A 1, 2
Malakhova Maja V. 3
Yudin Victor G 4
Kovalchuk Sergey 1
Zhuravlev Yuriy N 4
Ilina Elena N 3
Gabibov Alexander G. 1, 2
Smirnov Ivan 1, 2
Publication typeJournal Article
Publication date2022-01-21
Quartile SCImago
Q1
Quartile WOS
Q1
Impact factor5.6
ISSN16616596, 14220067
PubMed ID:  35163108
Catalysis
Organic Chemistry
Inorganic Chemistry
Physical and Theoretical Chemistry
Computer Science Applications
Spectroscopy
Molecular Biology
General Medicine
Abstract

The biodiversity of microorganisms is maintained by intricate nets of interactions between competing species. Impaired functionality of human microbiomes correlates with their reduced biodiversity originating from aseptic environmental conditions and antibiotic use. Microbiomes of wild animals are free of these selective pressures. Microbiota provides a protecting shield from invasion by pathogens in the wild, outcompeting their growth in specific ecological niches. We applied ultrahigh-throughput microfluidic technologies for functional profiling of microbiomes of wild animals, including the skin beetle, Siberian lynx, common raccoon dog, and East Siberian brown bear. Single-cell screening of the most efficient killers of the common human pathogen Staphylococcus aureus resulted in repeated isolation of Bacillus pumilus strains. While isolated strains had different phenotypes, all of them displayed a similar set of biosynthetic gene clusters (BGCs) encoding antibiotic amicoumacin, siderophore bacillibactin, and putative analogs of antimicrobials including bacilysin, surfactin, desferrioxamine, and class IId cyclical bacteriocin. Amicoumacin A (Ami) was identified as a major antibacterial metabolite of these strains mediating their antagonistic activity. Genome mining indicates that Ami BGCs with this architecture subdivide into three distinct families, characteristic of the B. pumilus, B. subtilis, and Paenibacillus species. While Ami itself displays mediocre activity against the majority of Gram-negative bacteria, isolated B. pumilus strains efficiently inhibit the growth of both Gram-positive S. aureus and Gram-negative E. coli in coculture. We believe that the expanded antagonistic activity spectrum of Ami-producing B. pumilus can be attributed to the metabolomic profile predetermined by their biosynthetic fingerprint. Ultrahigh-throughput isolation of natural probiotic strains from wild animal microbiomes, as well as their metabolic reprogramming, opens up a new avenue for pathogen control and microbiome remodeling in the food industry, agriculture, and healthcare.

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GOST Copy
Baranova M. N. et al. Deep Functional Profiling of Wild Animal Microbiomes Reveals Probiotic Bacillus pumilus Strains with a Common Biosynthetic Fingerprint // International Journal of Molecular Sciences. 2022. Vol. 23. No. 3. p. 1168.
GOST all authors (up to 50) Copy
Baranova M. N., Kudzhaev A. M., Mokrushina Y. A., Babenko V., Kornienko M. A., Malakhova M. V., Yudin V. G., Rubtsova M. P., Zalevsky A., Belozerova O. A., Kovalchuk S., Zhuravlev Y. N., Ilina E. N., Gabibov A. G., Smirnov I., Terekhov S. S. Deep Functional Profiling of Wild Animal Microbiomes Reveals Probiotic Bacillus pumilus Strains with a Common Biosynthetic Fingerprint // International Journal of Molecular Sciences. 2022. Vol. 23. No. 3. p. 1168.
RIS |
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RIS Copy
TY - JOUR
DO - 10.3390/ijms23031168
UR - https://doi.org/10.3390%2Fijms23031168
TI - Deep Functional Profiling of Wild Animal Microbiomes Reveals Probiotic Bacillus pumilus Strains with a Common Biosynthetic Fingerprint
T2 - International Journal of Molecular Sciences
AU - Baranova, Margarita N
AU - Malakhova, Maja V.
AU - Yudin, Victor G
AU - Rubtsova, Maria P
AU - Kovalchuk, Sergey
AU - Zhuravlev, Yuriy N
AU - Ilina, Elena N
AU - Mokrushina, Yuliana A
AU - Gabibov, Alexander G.
AU - Kudzhaev, Arsen M
AU - Babenko, Vladislav
AU - Kornienko, Maria A
AU - Zalevsky, A.O.
AU - Belozerova, Olga A
AU - Smirnov, Ivan
AU - Terekhov, Stanislav S
PY - 2022
DA - 2022/01/21 00:00:00
PB - Multidisciplinary Digital Publishing Institute (MDPI)
SP - 1168
IS - 3
VL - 23
PMID - 35163108
SN - 1661-6596
SN - 1422-0067
ER -
BibTex |
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BibTex Copy
@article{2022_Baranova
author = {Margarita N Baranova and Maja V. Malakhova and Victor G Yudin and Maria P Rubtsova and Sergey Kovalchuk and Yuriy N Zhuravlev and Elena N Ilina and Yuliana A Mokrushina and Alexander G. Gabibov and Arsen M Kudzhaev and Vladislav Babenko and Maria A Kornienko and A.O. Zalevsky and Olga A Belozerova and Ivan Smirnov and Stanislav S Terekhov},
title = {Deep Functional Profiling of Wild Animal Microbiomes Reveals Probiotic Bacillus pumilus Strains with a Common Biosynthetic Fingerprint},
journal = {International Journal of Molecular Sciences},
year = {2022},
volume = {23},
publisher = {Multidisciplinary Digital Publishing Institute (MDPI)},
month = {jan},
url = {https://doi.org/10.3390%2Fijms23031168},
number = {3},
pages = {1168},
doi = {10.3390/ijms23031168}
}
MLA
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MLA Copy
Baranova, Margarita N., et al. “Deep Functional Profiling of Wild Animal Microbiomes Reveals Probiotic Bacillus pumilus Strains with a Common Biosynthetic Fingerprint.” International Journal of Molecular Sciences, vol. 23, no. 3, Jan. 2022, p. 1168. https://doi.org/10.3390%2Fijms23031168.
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