Modeling aerotaxis band formation in Azospirillum brasilense

Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes...

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Published inBMC microbiology Vol. 19; no. 1; pp. 101 - 10
Main Authors Elmas, Mustafa, Alexiades, Vasilios, O’Neal, Lindsey, Alexandre, Gladys
Format Journal Article
LanguageEnglish
Published London BioMed Central 17.05.2019
BioMed Central Ltd
BMC
Subjects
Aerotaxis
Azospirillum brasilense
Azospirillum brasilense - growth & development
Azospirillum brasilense - metabolism
Bacteria
Band formation
Biological Microscopy
Biomedical and Life Sciences
Cells (Biology)
Chemotaxis
Colonization
Concentration gradient
Crop production
E coli
Energy
Life Sciences
Limiting nutrients
Mathematical modeling
Mathematical models
Metabolism
Microbial biochemistry
Microbiology
Models, Theoretical
Motility
Mycology
Nutrients
Organic chemistry
Organisms
Oxygen
Oxygen - metabolism
Oxygen consumption
Parameter estimation
Parasitology
physiology and metabolism
Plant growth
Production management
Proteobacteria
Research Article
Rhizosphere
Soil bacteria
Soil microbiology
Soil microorganisms
Virology
Azospirillum brasilense
Band formation
Mathematical modeling
Aerotaxis
Chemotaxis
Online AccessGet full text
ISSN1471-2180
1471-2180
DOI10.1186/s12866-019-1468-9

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Abstract Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes the rhizosphere and promotes the growth of diverse plants across a range of environments. Aerotaxis, or the ability to navigate oxygen gradients, is a widespread behavior in bacteria. It is one of the strongest behavioral responses in A. brasilense and it is essential for successful colonization of the root surface. Oxygen is one of the limiting nutrients in the rhizosphere where density and activity of organisms are greatest. The aerotaxis response of A. brasilense is also characterized by high precision with motile cells able to detect narrow regions in a gradient where the oxygen concentration is low enough to support their microaerobic lifestyle and metabolism. Results Here, we present a mathematical model for aerotaxis band formation that captures most critical features of aerotaxis in A. brasilense . Remarkably, this model recapitulates experimental observations of the formation of a stable aerotactic band within 2 minutes of exposure to the air gradient that were not captured in previous modeling efforts. Using experimentally determined parameters, the mathematical model reproduced an aerotactic band at a distance from the meniscus and with a width that matched the experimental observation. Conclusions Including experimentally determined parameter values allowed us to validate a mathematical model for aerotactic band formation in spatial gradients that recapitulates the spatiotemporal stability of the band and its position in the gradient as well as its overall width. This validated model also allowed us to capture the range of oxygen concentrations the bacteria prefer during aerotaxis, and to estimate the effect of parameter values (e.g. oxygen consumption rate), both of which are difficult to obtain in experiments.
AbstractList Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes the rhizosphere and promotes the growth of diverse plants across a range of environments. Aerotaxis, or the ability to navigate oxygen gradients, is a widespread behavior in bacteria. It is one of the strongest behavioral responses in A. brasilense and it is essential for successful colonization of the root surface. Oxygen is one of the limiting nutrients in the rhizosphere where density and activity of organisms are greatest. The aerotaxis response of A. brasilense is also characterized by high precision with motile cells able to detect narrow regions in a gradient where the oxygen concentration is low enough to support their microaerobic lifestyle and metabolism. Results Here, we present a mathematical model for aerotaxis band formation that captures most critical features of aerotaxis in A. brasilense . Remarkably, this model recapitulates experimental observations of the formation of a stable aerotactic band within 2 minutes of exposure to the air gradient that were not captured in previous modeling efforts. Using experimentally determined parameters, the mathematical model reproduced an aerotactic band at a distance from the meniscus and with a width that matched the experimental observation. Conclusions Including experimentally determined parameter values allowed us to validate a mathematical model for aerotactic band formation in spatial gradients that recapitulates the spatiotemporal stability of the band and its position in the gradient as well as its overall width. This validated model also allowed us to capture the range of oxygen concentrations the bacteria prefer during aerotaxis, and to estimate the effect of parameter values (e.g. oxygen consumption rate), both of which are difficult to obtain in experiments.
Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes the rhizosphere and promotes the growth of diverse plants across a range of environments. Aerotaxis, or the ability to navigate oxygen gradients, is a widespread behavior in bacteria. It is one of the strongest behavioral responses in A. brasilense and it is essential for successful colonization of the root surface. Oxygen is one of the limiting nutrients in the rhizosphere where density and activity of organisms are greatest. The aerotaxis response of A. brasilense is also characterized by high precision with motile cells able to detect narrow regions in a gradient where the oxygen concentration is low enough to support their microaerobic lifestyle and metabolism. Here, we present a mathematical model for aerotaxis band formation that captures most critical features of aerotaxis in A. brasilense. Remarkably, this model recapitulates experimental observations of the formation of a stable aerotactic band within 2 minutes of exposure to the air gradient that were not captured in previous modeling efforts. Using experimentally determined parameters, the mathematical model reproduced an aerotactic band at a distance from the meniscus and with a width that matched the experimental observation. Including experimentally determined parameter values allowed us to validate a mathematical model for aerotactic band formation in spatial gradients that recapitulates the spatiotemporal stability of the band and its position in the gradient as well as its overall width. This validated model also allowed us to capture the range of oxygen concentrations the bacteria prefer during aerotaxis, and to estimate the effect of parameter values (e.g. oxygen consumption rate), both of which are difficult to obtain in experiments.
Abstract Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes the rhizosphere and promotes the growth of diverse plants across a range of environments. Aerotaxis, or the ability to navigate oxygen gradients, is a widespread behavior in bacteria. It is one of the strongest behavioral responses in A. brasilense and it is essential for successful colonization of the root surface. Oxygen is one of the limiting nutrients in the rhizosphere where density and activity of organisms are greatest. The aerotaxis response of A. brasilense is also characterized by high precision with motile cells able to detect narrow regions in a gradient where the oxygen concentration is low enough to support their microaerobic lifestyle and metabolism. Results Here, we present a mathematical model for aerotaxis band formation that captures most critical features of aerotaxis in A. brasilense. Remarkably, this model recapitulates experimental observations of the formation of a stable aerotactic band within 2 minutes of exposure to the air gradient that were not captured in previous modeling efforts. Using experimentally determined parameters, the mathematical model reproduced an aerotactic band at a distance from the meniscus and with a width that matched the experimental observation. Conclusions Including experimentally determined parameter values allowed us to validate a mathematical model for aerotactic band formation in spatial gradients that recapitulates the spatiotemporal stability of the band and its position in the gradient as well as its overall width. This validated model also allowed us to capture the range of oxygen concentrations the bacteria prefer during aerotaxis, and to estimate the effect of parameter values (e.g. oxygen consumption rate), both of which are difficult to obtain in experiments.
Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes the rhizosphere and promotes the growth of diverse plants across a range of environments. Aerotaxis, or the ability to navigate oxygen gradients, is a widespread behavior in bacteria. It is one of the strongest behavioral responses in A. brasilense and it is essential for successful colonization of the root surface. Oxygen is one of the limiting nutrients in the rhizosphere where density and activity of organisms are greatest. The aerotaxis response of A. brasilense is also characterized by high precision with motile cells able to detect narrow regions in a gradient where the oxygen concentration is low enough to support their microaerobic lifestyle and metabolism. Here, we present a mathematical model for aerotaxis band formation that captures most critical features of aerotaxis in A. brasilense. Remarkably, this model recapitulates experimental observations of the formation of a stable aerotactic band within 2 minutes of exposure to the air gradient that were not captured in previous modeling efforts. Using experimentally determined parameters, the mathematical model reproduced an aerotactic band at a distance from the meniscus and with a width that matched the experimental observation. Including experimentally determined parameter values allowed us to validate a mathematical model for aerotactic band formation in spatial gradients that recapitulates the spatiotemporal stability of the band and its position in the gradient as well as its overall width. This validated model also allowed us to capture the range of oxygen concentrations the bacteria prefer during aerotaxis, and to estimate the effect of parameter values (e.g. oxygen consumption rate), both of which are difficult to obtain in experiments.
Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes the rhizosphere and promotes the growth of diverse plants across a range of environments. Aerotaxis, or the ability to navigate oxygen gradients, is a widespread behavior in bacteria. It is one of the strongest behavioral responses in A. brasilense and it is essential for successful colonization of the root surface. Oxygen is one of the limiting nutrients in the rhizosphere where density and activity of organisms are greatest. The aerotaxis response of A. brasilense is also characterized by high precision with motile cells able to detect narrow regions in a gradient where the oxygen concentration is low enough to support their microaerobic lifestyle and metabolism. Results Here, we present a mathematical model for aerotaxis band formation that captures most critical features of aerotaxis in A. brasilense. Remarkably, this model recapitulates experimental observations of the formation of a stable aerotactic band within 2 minutes of exposure to the air gradient that were not captured in previous modeling efforts. Using experimentally determined parameters, the mathematical model reproduced an aerotactic band at a distance from the meniscus and with a width that matched the experimental observation. Conclusions Including experimentally determined parameter values allowed us to validate a mathematical model for aerotactic band formation in spatial gradients that recapitulates the spatiotemporal stability of the band and its position in the gradient as well as its overall width. This validated model also allowed us to capture the range of oxygen concentrations the bacteria prefer during aerotaxis, and to estimate the effect of parameter values (e.g. oxygen consumption rate), both of which are difficult to obtain in experiments.
Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes the rhizosphere and promotes the growth of diverse plants across a range of environments. Aerotaxis, or the ability to navigate oxygen gradients, is a widespread behavior in bacteria. It is one of the strongest behavioral responses in A. brasilense and it is essential for successful colonization of the root surface. Oxygen is one of the limiting nutrients in the rhizosphere where density and activity of organisms are greatest. The aerotaxis response of A. brasilense is also characterized by high precision with motile cells able to detect narrow regions in a gradient where the oxygen concentration is low enough to support their microaerobic lifestyle and metabolism. Results Here, we present a mathematical model for aerotaxis band formation that captures most critical features of aerotaxis in A. brasilense. Remarkably, this model recapitulates experimental observations of the formation of a stable aerotactic band within 2 minutes of exposure to the air gradient that were not captured in previous modeling efforts. Using experimentally determined parameters, the mathematical model reproduced an aerotactic band at a distance from the meniscus and with a width that matched the experimental observation. Conclusions Including experimentally determined parameter values allowed us to validate a mathematical model for aerotactic band formation in spatial gradients that recapitulates the spatiotemporal stability of the band and its position in the gradient as well as its overall width. This validated model also allowed us to capture the range of oxygen concentrations the bacteria prefer during aerotaxis, and to estimate the effect of parameter values (e.g. oxygen consumption rate), both of which are difficult to obtain in experiments. Keywords: Chemotaxis, Aerotaxis, Band formation, Azospirillum brasilense, Mathematical modeling
Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes the rhizosphere and promotes the growth of diverse plants across a range of environments. Aerotaxis, or the ability to navigate oxygen gradients, is a widespread behavior in bacteria. It is one of the strongest behavioral responses in A. brasilense and it is essential for successful colonization of the root surface. Oxygen is one of the limiting nutrients in the rhizosphere where density and activity of organisms are greatest. The aerotaxis response of A. brasilense is also characterized by high precision with motile cells able to detect narrow regions in a gradient where the oxygen concentration is low enough to support their microaerobic lifestyle and metabolism.BACKGROUNDBacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe associations, including those that benefit plant growth and crop productivity. The motile soil bacterium Azospirillum brasilense colonizes the rhizosphere and promotes the growth of diverse plants across a range of environments. Aerotaxis, or the ability to navigate oxygen gradients, is a widespread behavior in bacteria. It is one of the strongest behavioral responses in A. brasilense and it is essential for successful colonization of the root surface. Oxygen is one of the limiting nutrients in the rhizosphere where density and activity of organisms are greatest. The aerotaxis response of A. brasilense is also characterized by high precision with motile cells able to detect narrow regions in a gradient where the oxygen concentration is low enough to support their microaerobic lifestyle and metabolism.Here, we present a mathematical model for aerotaxis band formation that captures most critical features of aerotaxis in A. brasilense. Remarkably, this model recapitulates experimental observations of the formation of a stable aerotactic band within 2 minutes of exposure to the air gradient that were not captured in previous modeling efforts. Using experimentally determined parameters, the mathematical model reproduced an aerotactic band at a distance from the meniscus and with a width that matched the experimental observation.RESULTSHere, we present a mathematical model for aerotaxis band formation that captures most critical features of aerotaxis in A. brasilense. Remarkably, this model recapitulates experimental observations of the formation of a stable aerotactic band within 2 minutes of exposure to the air gradient that were not captured in previous modeling efforts. Using experimentally determined parameters, the mathematical model reproduced an aerotactic band at a distance from the meniscus and with a width that matched the experimental observation.Including experimentally determined parameter values allowed us to validate a mathematical model for aerotactic band formation in spatial gradients that recapitulates the spatiotemporal stability of the band and its position in the gradient as well as its overall width. This validated model also allowed us to capture the range of oxygen concentrations the bacteria prefer during aerotaxis, and to estimate the effect of parameter values (e.g. oxygen consumption rate), both of which are difficult to obtain in experiments.CONCLUSIONSIncluding experimentally determined parameter values allowed us to validate a mathematical model for aerotactic band formation in spatial gradients that recapitulates the spatiotemporal stability of the band and its position in the gradient as well as its overall width. This validated model also allowed us to capture the range of oxygen concentrations the bacteria prefer during aerotaxis, and to estimate the effect of parameter values (e.g. oxygen consumption rate), both of which are difficult to obtain in experiments.
ArticleNumber 101
Audience Academic
Author Alexiades, Vasilios
O’Neal, Lindsey
Alexandre, Gladys
Elmas, Mustafa
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  surname: Alexandre
  fullname: Alexandre, Gladys
  email: galexan2@utk.edu
  organization: Biochemistry and Cellular & Molecular Biology, University of Tennessee
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31101077$$D View this record in MEDLINE/PubMed
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Issue 1
Keywords Azospirillum brasilense
Band formation
Mathematical modeling
Aerotaxis
Chemotaxis
Language English
License Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License(http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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Snippet Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various...
Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various plant-microbe...
Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various...
Abstract Background Bacterial chemotaxis, the ability of motile bacteria to navigate gradients of chemicals, plays key roles in the establishment of various...
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StartPage 101
SubjectTerms Aerotaxis
Azospirillum brasilense
Azospirillum brasilense - growth & development
Azospirillum brasilense - metabolism
Bacteria
Band formation
Biological Microscopy
Biomedical and Life Sciences
Cells (Biology)
Chemotaxis
Colonization
Concentration gradient
Crop production
E coli
Energy
Life Sciences
Limiting nutrients
Mathematical modeling
Mathematical models
Metabolism
Microbial biochemistry
Microbiology
Models, Theoretical
Motility
Mycology
Nutrients
Organic chemistry
Organisms
Oxygen
Oxygen - metabolism
Oxygen consumption
Parameter estimation
Parasitology
physiology and metabolism
Plant growth
Production management
Proteobacteria
Research Article
Rhizosphere
Soil bacteria
Soil microbiology
Soil microorganisms
Virology
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Title Modeling aerotaxis band formation in Azospirillum brasilense
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