Vibrio alginolyticus growth kinetics and the metabolic effects of iron
ABSTRACT Vibrio alginolyticus is a naturally occurring marine bacterium, recognized as an emerging pathogen in humans and animals and the second most common cause of vibriosis in the U.S. However, information regarding the physiology and growth of this species in the environment is limited. Here we...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-12-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02680-23 |
| _version_ | 1797393678686224384 |
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| author | William A. Norfolk Charlyn Shue W. Matthew Henderson Donna A. Glinski Erin K. Lipp |
| author_facet | William A. Norfolk Charlyn Shue W. Matthew Henderson Donna A. Glinski Erin K. Lipp |
| author_sort | William A. Norfolk |
| collection | DOAJ |
| description | ABSTRACT Vibrio alginolyticus is a naturally occurring marine bacterium, recognized as an emerging pathogen in humans and animals and the second most common cause of vibriosis in the U.S. However, information regarding the physiology and growth of this species in the environment is limited. Here we evaluated the effects of temperature, salinity, and iron condition on the growth response across unique V. alginolyticus strains. A combination of growth kinetics and gas chromatography-mass spectrometry-based metabolomics studies was used to evaluate the optimal and tolerable ranges of growth and to characterize the metabolic effects of iron supplementation. All V. alginolyticus strains tested demonstrated broad temperature and salinity tolerance, resulting in growth at all measured temperatures (24°C–40°C) and salinities between 1% and 6% (wt/vol) NaCl with optimal growth between 30°C–36°C and 2%–4% NaCl. Environmental strains showed no growth limitation at iron concentrations ranging from 0.5- to 20.0-µM ferric Fe but demonstrated reduced growth at 0.2 µM. Likewise, the number of significantly upregulated metabolites in V. alginolyticus cultures grown in iron-replete (4-µM) media was greater than that in iron-deficient (~0 µM) media but varied with prior growth conditions. Detected compounds were associated with key metabolic pathways, namely, amino acid, carbohydrate, lipid, and nucleotide metabolism, suggesting that introduced iron facilitated broad activation of V. alginolyticus metabolism and helped to promote growth responses. Combined, these results demonstrate that V. alginolyticus strains are capable of rapid growth under a broad range of favorable temperature and salinity levels, which can be affected by the presence of iron. IMPORTANCE Transmission of V. alginolyticus occurs opportunistically through direct seawater exposure and is a function of its abundance in the environment. Like other Vibrio spp., V. alginolyticus are considered conditionally rare taxa in marine waters, with populations capable of forming large, short-lived blooms under specific environmental conditions, which remain poorly defined. Prior research has established the importance of temperature and salinity as the major determinants of Vibrio geographical and temporal range. However, bloom formation can be strongly influenced by other factors that may be more episodic and localized, such as changes in iron availability. Here we confirm the broad temperature and salinity tolerance of V. alginolyticus and demonstrate the importance of iron supplementation as a key factor for growth in the absence of thermal or osmotic stress. The results of this research highlight the importance of episodic iron input as a crucial metric to consider for the assessment of V. alginolyticus risk. |
| first_indexed | 2024-03-09T00:06:20Z |
| format | Article |
| id | doaj.art-81420914a672403fae32b32aad9f80b8 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-09T00:06:20Z |
| publishDate | 2023-12-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-81420914a672403fae32b32aad9f80b82023-12-12T13:17:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-12-0111610.1128/spectrum.02680-23Vibrio alginolyticus growth kinetics and the metabolic effects of ironWilliam A. Norfolk0Charlyn Shue1W. Matthew Henderson2Donna A. Glinski3Erin K. Lipp4Department of Environmental Health Science, University of Georgia , Athens, Georgia, USADepartment of Environmental Health Science, University of Georgia , Athens, Georgia, USAU.S. Environmental Protection Agency, Office of Research and Development, Center for Environmental Measurement and Modeling , Athens, Georgia, USAU.S. Environmental Protection Agency, Office of Research and Development, Center for Environmental Measurement and Modeling , Athens, Georgia, USADepartment of Environmental Health Science, University of Georgia , Athens, Georgia, USAABSTRACT Vibrio alginolyticus is a naturally occurring marine bacterium, recognized as an emerging pathogen in humans and animals and the second most common cause of vibriosis in the U.S. However, information regarding the physiology and growth of this species in the environment is limited. Here we evaluated the effects of temperature, salinity, and iron condition on the growth response across unique V. alginolyticus strains. A combination of growth kinetics and gas chromatography-mass spectrometry-based metabolomics studies was used to evaluate the optimal and tolerable ranges of growth and to characterize the metabolic effects of iron supplementation. All V. alginolyticus strains tested demonstrated broad temperature and salinity tolerance, resulting in growth at all measured temperatures (24°C–40°C) and salinities between 1% and 6% (wt/vol) NaCl with optimal growth between 30°C–36°C and 2%–4% NaCl. Environmental strains showed no growth limitation at iron concentrations ranging from 0.5- to 20.0-µM ferric Fe but demonstrated reduced growth at 0.2 µM. Likewise, the number of significantly upregulated metabolites in V. alginolyticus cultures grown in iron-replete (4-µM) media was greater than that in iron-deficient (~0 µM) media but varied with prior growth conditions. Detected compounds were associated with key metabolic pathways, namely, amino acid, carbohydrate, lipid, and nucleotide metabolism, suggesting that introduced iron facilitated broad activation of V. alginolyticus metabolism and helped to promote growth responses. Combined, these results demonstrate that V. alginolyticus strains are capable of rapid growth under a broad range of favorable temperature and salinity levels, which can be affected by the presence of iron. IMPORTANCE Transmission of V. alginolyticus occurs opportunistically through direct seawater exposure and is a function of its abundance in the environment. Like other Vibrio spp., V. alginolyticus are considered conditionally rare taxa in marine waters, with populations capable of forming large, short-lived blooms under specific environmental conditions, which remain poorly defined. Prior research has established the importance of temperature and salinity as the major determinants of Vibrio geographical and temporal range. However, bloom formation can be strongly influenced by other factors that may be more episodic and localized, such as changes in iron availability. Here we confirm the broad temperature and salinity tolerance of V. alginolyticus and demonstrate the importance of iron supplementation as a key factor for growth in the absence of thermal or osmotic stress. The results of this research highlight the importance of episodic iron input as a crucial metric to consider for the assessment of V. alginolyticus risk.https://journals.asm.org/doi/10.1128/spectrum.02680-23Vibrio alginolyticusironphysiologymetabolomicsgrowth kineticstolerance |
| spellingShingle | William A. Norfolk Charlyn Shue W. Matthew Henderson Donna A. Glinski Erin K. Lipp Vibrio alginolyticus growth kinetics and the metabolic effects of iron Microbiology Spectrum Vibrio alginolyticus iron physiology metabolomics growth kinetics tolerance |
| title | Vibrio alginolyticus growth kinetics and the metabolic effects of iron |
| title_full | Vibrio alginolyticus growth kinetics and the metabolic effects of iron |
| title_fullStr | Vibrio alginolyticus growth kinetics and the metabolic effects of iron |
| title_full_unstemmed | Vibrio alginolyticus growth kinetics and the metabolic effects of iron |
| title_short | Vibrio alginolyticus growth kinetics and the metabolic effects of iron |
| title_sort | vibrio alginolyticus growth kinetics and the metabolic effects of iron |
| topic | Vibrio alginolyticus iron physiology metabolomics growth kinetics tolerance |
| url | https://journals.asm.org/doi/10.1128/spectrum.02680-23 |
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