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Differential Effects of Transition Metals on Growth and Metal Uptake for Two Distinct Lactobacillus Species

Lactobacillus is a genus of Gram-positive bacteria and comprises a major part of the lactic acid bacteria group that converts sugars to lactic acid. Lactobacillus species found in the gut microbiota are considered beneficial to human health and commonly used in probiotic formulations, but their mole...

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Autores principales: Huynh, Uyen, Qiao, Muxin, King, John, Trinh, Brittany, Valdez, Juventino, Haq, Marium, Zastrow, Melissa L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8791193/
https://www.ncbi.nlm.nih.gov/pubmed/35080431
http://dx.doi.org/10.1128/spectrum.01006-21
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author Huynh, Uyen
Qiao, Muxin
King, John
Trinh, Brittany
Valdez, Juventino
Haq, Marium
Zastrow, Melissa L.
author_facet Huynh, Uyen
Qiao, Muxin
King, John
Trinh, Brittany
Valdez, Juventino
Haq, Marium
Zastrow, Melissa L.
author_sort Huynh, Uyen
collection PubMed
description Lactobacillus is a genus of Gram-positive bacteria and comprises a major part of the lactic acid bacteria group that converts sugars to lactic acid. Lactobacillus species found in the gut microbiota are considered beneficial to human health and commonly used in probiotic formulations, but their molecular functions remain poorly defined. Microbes require metal ions for growth and function and must acquire them from the surrounding environment. Therefore, lactobacilli need to compete with other gut microbes for these nutrients, although their metal requirements are not well-understood. Indeed, the abundance of lactobacilli in the microbiota is frequently affected by dietary intake of essential metals like zinc, manganese, and iron, but few studies have investigated the role of metals, especially zinc, in the physiology and metabolism of Lactobacillus species. Here, we investigated metal uptake by quantifying total cellular metal contents and compared how transition metals affect the growth of two distinct Lactobacillus species, Lactobacillus plantarum ATCC 14917 and Lactobacillus acidophilus ATCC 4356. When grown in rich or metal-limited medium, both species took up more manganese, zinc, and iron compared with other transition metals measured. Distinct zinc-, manganese- and iron-dependent patterns were observed in the growth kinetics for these species and while certain levels of each metal promoted the growth kinetics of both Lactobacillus species, the effects depend significantly on the culture medium and growth conditions. IMPORTANCE The gastrointestinal tract contains trillions of microorganisms, which are central to human health. Lactobacilli are considered beneficial microbiota members and are often used in probiotics, but their molecular functions, and especially those which are metal-dependent, remain poorly defined. Abundance of lactobacilli in the microbiota is frequently affected by dietary intake of essential metals like manganese, zinc, and iron, but results are complex, sometimes contradictory, and poorly predictable. There is a significant need to understand how host diet and metabolism will affect the microbiota, given that changes in microbiota composition are linked with disease and infection. The significance of our research is in gaining insight to how metals distinctly affect individual Lactobacillus species, which could lead to novel therapeutics and improved medical treatment. Growth kinetics and quantification of metal contents highlights how distinct species can respond differently to varied metal availability and provide a foundation for future molecular and mechanistic studies.
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spelling pubmed-87911932022-02-09 Differential Effects of Transition Metals on Growth and Metal Uptake for Two Distinct Lactobacillus Species Huynh, Uyen Qiao, Muxin King, John Trinh, Brittany Valdez, Juventino Haq, Marium Zastrow, Melissa L. Microbiol Spectr Research Article Lactobacillus is a genus of Gram-positive bacteria and comprises a major part of the lactic acid bacteria group that converts sugars to lactic acid. Lactobacillus species found in the gut microbiota are considered beneficial to human health and commonly used in probiotic formulations, but their molecular functions remain poorly defined. Microbes require metal ions for growth and function and must acquire them from the surrounding environment. Therefore, lactobacilli need to compete with other gut microbes for these nutrients, although their metal requirements are not well-understood. Indeed, the abundance of lactobacilli in the microbiota is frequently affected by dietary intake of essential metals like zinc, manganese, and iron, but few studies have investigated the role of metals, especially zinc, in the physiology and metabolism of Lactobacillus species. Here, we investigated metal uptake by quantifying total cellular metal contents and compared how transition metals affect the growth of two distinct Lactobacillus species, Lactobacillus plantarum ATCC 14917 and Lactobacillus acidophilus ATCC 4356. When grown in rich or metal-limited medium, both species took up more manganese, zinc, and iron compared with other transition metals measured. Distinct zinc-, manganese- and iron-dependent patterns were observed in the growth kinetics for these species and while certain levels of each metal promoted the growth kinetics of both Lactobacillus species, the effects depend significantly on the culture medium and growth conditions. IMPORTANCE The gastrointestinal tract contains trillions of microorganisms, which are central to human health. Lactobacilli are considered beneficial microbiota members and are often used in probiotics, but their molecular functions, and especially those which are metal-dependent, remain poorly defined. Abundance of lactobacilli in the microbiota is frequently affected by dietary intake of essential metals like manganese, zinc, and iron, but results are complex, sometimes contradictory, and poorly predictable. There is a significant need to understand how host diet and metabolism will affect the microbiota, given that changes in microbiota composition are linked with disease and infection. The significance of our research is in gaining insight to how metals distinctly affect individual Lactobacillus species, which could lead to novel therapeutics and improved medical treatment. Growth kinetics and quantification of metal contents highlights how distinct species can respond differently to varied metal availability and provide a foundation for future molecular and mechanistic studies. American Society for Microbiology 2022-01-26 /pmc/articles/PMC8791193/ /pubmed/35080431 http://dx.doi.org/10.1128/spectrum.01006-21 Text en Copyright © 2022 Huynh et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Huynh, Uyen
Qiao, Muxin
King, John
Trinh, Brittany
Valdez, Juventino
Haq, Marium
Zastrow, Melissa L.
Differential Effects of Transition Metals on Growth and Metal Uptake for Two Distinct Lactobacillus Species
title Differential Effects of Transition Metals on Growth and Metal Uptake for Two Distinct Lactobacillus Species
title_full Differential Effects of Transition Metals on Growth and Metal Uptake for Two Distinct Lactobacillus Species
title_fullStr Differential Effects of Transition Metals on Growth and Metal Uptake for Two Distinct Lactobacillus Species
title_full_unstemmed Differential Effects of Transition Metals on Growth and Metal Uptake for Two Distinct Lactobacillus Species
title_short Differential Effects of Transition Metals on Growth and Metal Uptake for Two Distinct Lactobacillus Species
title_sort differential effects of transition metals on growth and metal uptake for two distinct lactobacillus species
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8791193/
https://www.ncbi.nlm.nih.gov/pubmed/35080431
http://dx.doi.org/10.1128/spectrum.01006-21
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