Development of Nanoparticle Adaptation Phenomena in Acinetobacter baumannii: Physiological Change and Defense Response
ABSTRACT The present work describes the evolution of a resistance phenotype to a multitargeting antimicrobial agent, namely, silver nanoparticles (nanosilver; NAg), in the globally prevalent bacterial pathogen Acinetobacter baumannii. The Gram-negative bacterium has recently been listed as a critica...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-02-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02857-22 |
| _version_ | 1811164428240945152 |
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| author | Oliver McNeilly Riti Mann Max Laurence Cummins Steven P. Djordjevic Mehrad Hamidian Cindy Gunawan |
| author_facet | Oliver McNeilly Riti Mann Max Laurence Cummins Steven P. Djordjevic Mehrad Hamidian Cindy Gunawan |
| author_sort | Oliver McNeilly |
| collection | DOAJ |
| description | ABSTRACT The present work describes the evolution of a resistance phenotype to a multitargeting antimicrobial agent, namely, silver nanoparticles (nanosilver; NAg), in the globally prevalent bacterial pathogen Acinetobacter baumannii. The Gram-negative bacterium has recently been listed as a critical priority pathogen requiring novel treatment options by the World Health Organization. Through prolonged exposure to the important antimicrobial nanoparticle, the bacterium developed mutations in genes that encode the protein subunits of organelle structures that are involved in cell-to-surface attachment as well as in a cell envelope capsular polysaccharide synthesis-related gene. These mutations are potentially correlated with stable physiological changes in the biofilm growth behavior and with an evident protective effect against oxidative stress, most likely as a feature of toxicity defense. We further report a different adaptation response of A. baumannii to the cationic form of silver (Ag+). The bacterium developed a tolerance phenotype to Ag+, which was correlated with an indicative surge in respiratory activity and changes in cell morphology, of which these are reported characteristics of tolerant bacterial populations. The findings regarding adaptation phenomena to NAg highlight the risks of the long-term use of the nanoparticle on a priority pathogen. The findings urge the implementation of strategies to overcome bacterial NAg adaptation, to better elucidate the toxicity mechanisms of the nanoparticle, and preserve the efficacy of the potent alternative antimicrobial agent in this era of antimicrobial resistance. IMPORTANCE Several recent studies have reported on the development of bacterial resistance to broad-spectrum antimicrobial silver nanoparticles (nanosilver; NAg). NAg is currently one of the most important alternative antimicrobial agents. However, no studies have yet established whether Acinetobacter baumannii, a globally prevalent nosocomial pathogen, can develop resistance to the nanoparticle. The study herein describes how a model strain of A. baumannii with no inherent silver resistance determinants developed resistance to NAg, following prolonged exposure. The stable physiological changes are correlated with mutations detected in the bacterium genome. These mutations render the bacterium capable of proliferating at a toxic NAg concentration. It was also found that A. baumannii developed a “slower-to-kill” tolerance trait to Ag+, which highlights the unique antimicrobial activities between the nanoparticulate and the ionic forms of silver. Despite the proven efficacy of NAg, the observation of NAg resistance in A. baumannii emphasises the potential risks of the repeated overuse of this agent on a priority pathogen. |
| first_indexed | 2024-04-10T15:21:14Z |
| format | Article |
| id | doaj.art-2004b3913da7419a8cb49c7fa3b4411f |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-04-10T15:21:14Z |
| publishDate | 2023-02-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-2004b3913da7419a8cb49c7fa3b4411f2023-02-14T14:15:49ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-02-0111110.1128/spectrum.02857-22Development of Nanoparticle Adaptation Phenomena in Acinetobacter baumannii: Physiological Change and Defense ResponseOliver McNeilly0Riti Mann1Max Laurence Cummins2Steven P. Djordjevic3Mehrad Hamidian4Cindy Gunawan5Australian Institute of Microbiology and Infection, University of Technology Sydney, Broadway, New South Wales, AustraliaAustralian Institute of Microbiology and Infection, University of Technology Sydney, Broadway, New South Wales, AustraliaAustralian Institute of Microbiology and Infection, University of Technology Sydney, Broadway, New South Wales, AustraliaAustralian Institute of Microbiology and Infection, University of Technology Sydney, Broadway, New South Wales, AustraliaAustralian Institute of Microbiology and Infection, University of Technology Sydney, Broadway, New South Wales, AustraliaAustralian Institute of Microbiology and Infection, University of Technology Sydney, Broadway, New South Wales, AustraliaABSTRACT The present work describes the evolution of a resistance phenotype to a multitargeting antimicrobial agent, namely, silver nanoparticles (nanosilver; NAg), in the globally prevalent bacterial pathogen Acinetobacter baumannii. The Gram-negative bacterium has recently been listed as a critical priority pathogen requiring novel treatment options by the World Health Organization. Through prolonged exposure to the important antimicrobial nanoparticle, the bacterium developed mutations in genes that encode the protein subunits of organelle structures that are involved in cell-to-surface attachment as well as in a cell envelope capsular polysaccharide synthesis-related gene. These mutations are potentially correlated with stable physiological changes in the biofilm growth behavior and with an evident protective effect against oxidative stress, most likely as a feature of toxicity defense. We further report a different adaptation response of A. baumannii to the cationic form of silver (Ag+). The bacterium developed a tolerance phenotype to Ag+, which was correlated with an indicative surge in respiratory activity and changes in cell morphology, of which these are reported characteristics of tolerant bacterial populations. The findings regarding adaptation phenomena to NAg highlight the risks of the long-term use of the nanoparticle on a priority pathogen. The findings urge the implementation of strategies to overcome bacterial NAg adaptation, to better elucidate the toxicity mechanisms of the nanoparticle, and preserve the efficacy of the potent alternative antimicrobial agent in this era of antimicrobial resistance. IMPORTANCE Several recent studies have reported on the development of bacterial resistance to broad-spectrum antimicrobial silver nanoparticles (nanosilver; NAg). NAg is currently one of the most important alternative antimicrobial agents. However, no studies have yet established whether Acinetobacter baumannii, a globally prevalent nosocomial pathogen, can develop resistance to the nanoparticle. The study herein describes how a model strain of A. baumannii with no inherent silver resistance determinants developed resistance to NAg, following prolonged exposure. The stable physiological changes are correlated with mutations detected in the bacterium genome. These mutations render the bacterium capable of proliferating at a toxic NAg concentration. It was also found that A. baumannii developed a “slower-to-kill” tolerance trait to Ag+, which highlights the unique antimicrobial activities between the nanoparticulate and the ionic forms of silver. Despite the proven efficacy of NAg, the observation of NAg resistance in A. baumannii emphasises the potential risks of the repeated overuse of this agent on a priority pathogen.https://journals.asm.org/doi/10.1128/spectrum.02857-22Acinetobacter baumanniimutationresistancesilver nanoparticles |
| spellingShingle | Oliver McNeilly Riti Mann Max Laurence Cummins Steven P. Djordjevic Mehrad Hamidian Cindy Gunawan Development of Nanoparticle Adaptation Phenomena in Acinetobacter baumannii: Physiological Change and Defense Response Microbiology Spectrum Acinetobacter baumannii mutation resistance silver nanoparticles |
| title | Development of Nanoparticle Adaptation Phenomena in Acinetobacter baumannii: Physiological Change and Defense Response |
| title_full | Development of Nanoparticle Adaptation Phenomena in Acinetobacter baumannii: Physiological Change and Defense Response |
| title_fullStr | Development of Nanoparticle Adaptation Phenomena in Acinetobacter baumannii: Physiological Change and Defense Response |
| title_full_unstemmed | Development of Nanoparticle Adaptation Phenomena in Acinetobacter baumannii: Physiological Change and Defense Response |
| title_short | Development of Nanoparticle Adaptation Phenomena in Acinetobacter baumannii: Physiological Change and Defense Response |
| title_sort | development of nanoparticle adaptation phenomena in acinetobacter baumannii physiological change and defense response |
| topic | Acinetobacter baumannii mutation resistance silver nanoparticles |
| url | https://journals.asm.org/doi/10.1128/spectrum.02857-22 |
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