Beyond traditional screening: Unveiling antibiotic potentials of actinomycetes in extreme environments

Extreme ecosystems are a rich source of specialized metabolites that can overcome multidrug resistance. However, the low efficiency of traditional exploratory research in discovering new antibiotics remains a major limitation. We hypothesized that actinomycetes may have the ability to produce antibi...

Full description

Saved in:
Bibliographic Details
Main Authors: Lyudmila P. Trenozhnikova, Gul B. Baimakhanova, Baiken B. Baimakhanova, Assya S. Balgimbayeva, Saule T. Daugaliyeva, Elmira R. Faizulina, Larisa G. Tatarkina, Gulzhan A. Spankulova, Dmitriy A. Berillo, John A. Beutler
Format: Article
Language:English
Published: Elsevier 2024-11-01
Series:Heliyon
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S240584402416402X
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846148822976167936
author Lyudmila P. Trenozhnikova
Gul B. Baimakhanova
Baiken B. Baimakhanova
Assya S. Balgimbayeva
Saule T. Daugaliyeva
Elmira R. Faizulina
Larisa G. Tatarkina
Gulzhan A. Spankulova
Dmitriy A. Berillo
John A. Beutler
author_facet Lyudmila P. Trenozhnikova
Gul B. Baimakhanova
Baiken B. Baimakhanova
Assya S. Balgimbayeva
Saule T. Daugaliyeva
Elmira R. Faizulina
Larisa G. Tatarkina
Gulzhan A. Spankulova
Dmitriy A. Berillo
John A. Beutler
author_sort Lyudmila P. Trenozhnikova
collection DOAJ
description Extreme ecosystems are a rich source of specialized metabolites that can overcome multidrug resistance. However, the low efficiency of traditional exploratory research in discovering new antibiotics remains a major limitation. We hypothesized that actinomycetes may have the ability to produce antibiotics in the extremes of a changing natural environment. This study introduces a novel approach to screening natural antibiotic producers from extreme habitats based on the relationship between organisms' adaptive traits and their metabolic activities. The antibacterial and antifungal properties of 667 actinomycete isolates, obtained from 160 samples of Kazakhstan's diverse extreme habitats, were studied under neutral, saline, and alkaline conditions against MRSA, E. coli, C. albicans, and A. niger. Among these isolates, 113 exhibited antibacterial properties, and 109 demonstrated antifungal properties. Notably, one-fifth of the antagonist isolates could produce active substances solely under extreme growth conditions. Fifty-three antagonistic actinomycetes, possessing these characteristics, have been categorized into groups and warrant further investigation as potential producers of new natural antibiotics. Molecular genetic analysis of the selected isolates revealed a high prevalence of Streptomyces and Nocardiopsis strains. Furthermore, 83.4 % of obtained isolates demonstrated the ability to thrive in all studied habitats—neutral, saline, and alkaline. 96.3 % of actinomycetes isolated from extreme environments exhibited adaptation to neutral conditions, highlighting their inherent versatility. Our findings underscore the nearly complete potential (99.7 %) of isolates to overcome the salinity barrier of 3.5 % NaCl, indicating their capacity to inhabit oceanic environments. We assert that actinomycetes should be perceived as a cohesive, globally adaptive group, capable of migrating between changing conditions or remaining stable within them. These studies lay the groundwork for the development of a new platform for screening natural antibiotics.
format Article
id doaj-art-87b29d79ddd04cefaa443e7e279cad72
institution Kabale University
issn 2405-8440
language English
publishDate 2024-11-01
publisher Elsevier
record_format Article
series Heliyon
spelling doaj-art-87b29d79ddd04cefaa443e7e279cad722024-11-30T07:12:43ZengElsevierHeliyon2405-84402024-11-011022e40371Beyond traditional screening: Unveiling antibiotic potentials of actinomycetes in extreme environmentsLyudmila P. Trenozhnikova0Gul B. Baimakhanova1Baiken B. Baimakhanova2Assya S. Balgimbayeva3Saule T. Daugaliyeva4Elmira R. Faizulina5Larisa G. Tatarkina6Gulzhan A. Spankulova7Dmitriy A. Berillo8John A. Beutler9LLP Research and Production Center for Microbiology and Virology, Almaty, Republic of Kazakhstan, Kazakhstan; Corresponding author.LLP Research and Production Center for Microbiology and Virology, Almaty, Republic of Kazakhstan, KazakhstanLLP Research and Production Center for Microbiology and Virology, Almaty, Republic of Kazakhstan, KazakhstanLLP Research and Production Center for Microbiology and Virology, Almaty, Republic of Kazakhstan, KazakhstanLLP Research and Production Center for Microbiology and Virology, Almaty, Republic of Kazakhstan, KazakhstanLLP Research and Production Center for Microbiology and Virology, Almaty, Republic of Kazakhstan, KazakhstanLLP Research and Production Center for Microbiology and Virology, Almaty, Republic of Kazakhstan, KazakhstanLLP Research and Production Center for Microbiology and Virology, Almaty, Republic of Kazakhstan, KazakhstanDepartment of Chemistry and Biochemical Engineering, Satbayev University, Almaty, Republic of Kazakhstan, Kazakhstan; Department of Biochemistry, Asfendiyarov Kazakh National Medical University, Almaty, Republic of Kazakhstan, Kazakhstan; Corresponding author. Department of Chemistry and Biochemical Engineering, Satbayev University, Almaty, Republic of Kazakhstan, Kazakhstan.Molecular Targets Program, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Frederick, MD, USAExtreme ecosystems are a rich source of specialized metabolites that can overcome multidrug resistance. However, the low efficiency of traditional exploratory research in discovering new antibiotics remains a major limitation. We hypothesized that actinomycetes may have the ability to produce antibiotics in the extremes of a changing natural environment. This study introduces a novel approach to screening natural antibiotic producers from extreme habitats based on the relationship between organisms' adaptive traits and their metabolic activities. The antibacterial and antifungal properties of 667 actinomycete isolates, obtained from 160 samples of Kazakhstan's diverse extreme habitats, were studied under neutral, saline, and alkaline conditions against MRSA, E. coli, C. albicans, and A. niger. Among these isolates, 113 exhibited antibacterial properties, and 109 demonstrated antifungal properties. Notably, one-fifth of the antagonist isolates could produce active substances solely under extreme growth conditions. Fifty-three antagonistic actinomycetes, possessing these characteristics, have been categorized into groups and warrant further investigation as potential producers of new natural antibiotics. Molecular genetic analysis of the selected isolates revealed a high prevalence of Streptomyces and Nocardiopsis strains. Furthermore, 83.4 % of obtained isolates demonstrated the ability to thrive in all studied habitats—neutral, saline, and alkaline. 96.3 % of actinomycetes isolated from extreme environments exhibited adaptation to neutral conditions, highlighting their inherent versatility. Our findings underscore the nearly complete potential (99.7 %) of isolates to overcome the salinity barrier of 3.5 % NaCl, indicating their capacity to inhabit oceanic environments. We assert that actinomycetes should be perceived as a cohesive, globally adaptive group, capable of migrating between changing conditions or remaining stable within them. These studies lay the groundwork for the development of a new platform for screening natural antibiotics.http://www.sciencedirect.com/science/article/pii/S240584402416402XExtreme habitatsNovel screening approachActinomycetesAdaptabilityAntibiotics
spellingShingle Lyudmila P. Trenozhnikova
Gul B. Baimakhanova
Baiken B. Baimakhanova
Assya S. Balgimbayeva
Saule T. Daugaliyeva
Elmira R. Faizulina
Larisa G. Tatarkina
Gulzhan A. Spankulova
Dmitriy A. Berillo
John A. Beutler
Beyond traditional screening: Unveiling antibiotic potentials of actinomycetes in extreme environments
Heliyon
Extreme habitats
Novel screening approach
Actinomycetes
Adaptability
Antibiotics
title Beyond traditional screening: Unveiling antibiotic potentials of actinomycetes in extreme environments
title_full Beyond traditional screening: Unveiling antibiotic potentials of actinomycetes in extreme environments
title_fullStr Beyond traditional screening: Unveiling antibiotic potentials of actinomycetes in extreme environments
title_full_unstemmed Beyond traditional screening: Unveiling antibiotic potentials of actinomycetes in extreme environments
title_short Beyond traditional screening: Unveiling antibiotic potentials of actinomycetes in extreme environments
title_sort beyond traditional screening unveiling antibiotic potentials of actinomycetes in extreme environments
topic Extreme habitats
Novel screening approach
Actinomycetes
Adaptability
Antibiotics
url http://www.sciencedirect.com/science/article/pii/S240584402416402X
work_keys_str_mv AT lyudmilaptrenozhnikova beyondtraditionalscreeningunveilingantibioticpotentialsofactinomycetesinextremeenvironments
AT gulbbaimakhanova beyondtraditionalscreeningunveilingantibioticpotentialsofactinomycetesinextremeenvironments
AT baikenbbaimakhanova beyondtraditionalscreeningunveilingantibioticpotentialsofactinomycetesinextremeenvironments
AT assyasbalgimbayeva beyondtraditionalscreeningunveilingantibioticpotentialsofactinomycetesinextremeenvironments
AT sauletdaugaliyeva beyondtraditionalscreeningunveilingantibioticpotentialsofactinomycetesinextremeenvironments
AT elmirarfaizulina beyondtraditionalscreeningunveilingantibioticpotentialsofactinomycetesinextremeenvironments
AT larisagtatarkina beyondtraditionalscreeningunveilingantibioticpotentialsofactinomycetesinextremeenvironments
AT gulzhanaspankulova beyondtraditionalscreeningunveilingantibioticpotentialsofactinomycetesinextremeenvironments
AT dmitriyaberillo beyondtraditionalscreeningunveilingantibioticpotentialsofactinomycetesinextremeenvironments
AT johnabeutler beyondtraditionalscreeningunveilingantibioticpotentialsofactinomycetesinextremeenvironments